smaller fleas

It was during smalltalk over a shared breakfast table on Amtrak that the man across from me began excoriating powdery mildew. He was a Colorado pot grower. His greenhouse operation held hundreds of plants, and the air circulating between his and the adjoining pot greenhouses was spreading the spores of the leaf parasitic fungus that had somehow gained a foothold inside. The greenhouse conditions provided an ideal environment for germination and growth of powdery mildew, and the high density of plants insured an endless supply of favorable landing spots for the dust-like particles that can each start a new colony. Despite the lore, pot plants are not indestructible, but rather serve as hosts to many pests and diseases, with powdery mildew being a leading factor threatening pot growers’ investment. Powdery mildew doesn’t kill a plant outright, but it weakens the plant and lowers the harvest quality.

There are about a hundred species of powdery mildew that make up this family of fungi. A powdery mildew’s thread-like growths cover the surface of a leaf and send root-like structures into the cells to feed. Its upright chains of spores give the impression of powder on the leaf. Powdery mildew is known as an “obligate biotroph”, meaning it can only survive on living host tissue. A key requirement of this infection type is that the fungus must come pre-programmed to neither kill the parasitized plant cell nor awaken the cell’s defense mechanisms, a balancing act accomplished through a tightly choreographed sequence of interactions with the cell’s machinery.

A reality of the plant world, though, is that distantly related plant species have distinct cellular machinery, meaning that a powdery mildew species that is not correctly pre-programmed, that is to say, coevolved with the plant it arrives on, will trip up and not be able to infect. Thus the powdery mildew on the sowthistle next door will not spread to your pumpkins, and the powdery mildew that emerges on the rosebush at the end of the row of grapevines and signals the grower to spray sulfur on the vines is not the species that actually infects the vines.

What the powdery mildew species have in common is similar germination requirements. The reason for this is that the spores carry their own moisture, allowing them to germinate without the liquid water that most fungal spores require. In fact, liquid water inhibits powdery mildew spore germination and can even cause the spores to burst. The spores do need a certain amount of humidity to germinate, but it can be as low as 50% relative humidity, and germination works better within a mild temperature range and at lower light levels. Outdoors there are certain times of year when powdery mildew blooms, but greenhouses are always ideal incubators waiting for spores to arrive.

For control of powdery mildew on grapevines, great quantities of sulfur and fungicides are sprayed, the most for any pathogen. However, since weed is newly legalized and gets smoked, growers don’t have an arsenal of chemicals registered for use on it. Cannabis pathologist Zamir Punja from British Columbia has found a few treatments to be effective, including Regalia, which is an extract of giant knotweed, Milstop, which is similar to baking soda but without the sodium, and germicidal ultraviolet light for a few seconds a day. There are some biocontrols that show promise as well. These mostly produce inhibitory chemicals or destructive enzymes against the fungus, or prime the plant to fight off infection, but a recent study from Hungary led by Márk Németh working in the lab of Levente Kiss shows the potential of a biocontrol agent that acts like a creature from science fiction.

In John Carpenter’s 1982 re-visioning of the sci fi classic The Thing, there is not monster played by a man in a suit as in the original, but instead a shape-shifting menace that lives inside its victims, compelling them to act in ways that benefit this alien life form while they retain their own personality. The most riveting scene is where the Kurt Russell character uses a flamethrower to kill a crew member carrying the parasite, which had revealed itself when it had burst out of his chest to engulf the arms of a comrade. The carrier is lying on a table as the flames sear his body, but his head hanging over the edge is out of direct exposure. To the horror of the crew and the audience alike, the head grows a stalk to lower itself to the ground then sprouts legs and tries to slink away. The film proceeds with an air of paranoia as crew members try to figure out who else may be harboring the monster.

The Thing was inspired by the atmosphere of fear and suspicion associated with the cold war, as were many if not all classic sci fi movies, but it could have been inspired by Ampelomyces. This fungus lives inside the tiny threads that make up the powdery mildew. It doesn’t kill the host fungus at first, but grows inside it, finally hijacking its reproductive structures to make more Ampelomyces. The tiny powdery mildew spores become filled with the even tinier spores of the hyperparasite, so-called because it is a parasite of a parasite.

The basic life history of Ampelomyces has been known since the nineteenth century, but Németh et al. have done the definitive study by engineering this fungus to glow green under blue light, allowing them to see its diminutive threads inside its host. They accomplished this using a gene from a jellyfish and a bacterium from a plant gall. The jellyfish is the bioluminescent crystal jelly of Puget Sound, which has a gene for producing green fluorescent protein. The bacterium is the pathogen responsible crown gall in plants, and it alters the growth of its host by inserting a plant tumor gene into the host’s DNA. The scientists replaced the bacterium’s tumor gene with the green fluorescent protein gene, added the bacterium to the fungus culture, and created the green-glowing fungus they were seeking.

One of the key questions that could be answered with an easily seen fungus was, what happens to it outside its host? It turns out that it can survive on a leaf surface for weeks after germination before any host comes along. Considering how utterly tiny the hyperparasite is, and the fact that it is not eating during that time, this is quite a feat. This feature is advantageous for harnessing it as a biocontrol agent, as a grower would not have to wait until a plant is suffering from a powdery mildew infestation to apply Ampelomyces spores. With some appropriate greenhouse trials this might become an additional tool in the pot grower’s toolbox.

Németh et al. also confirmed previous work showing that, unlike powdery mildew, Ampelomyces is not specific to a single host species, but is able grow within many different species of powdery mildew. This feature might make it amenable to conservation biocontrol, where the biocontrol agent is not raised commercially and sprayed onto the crop, but rather the agroecosystem is managed in such a way that hosts are always available for the biocontrol agent to survive on site. Perhaps a grower could leave sowthistles growing around the perimeter of the system to protect the pumpkins. Perhaps the rosebushes at the ends of the grapevine rows could serve not as early warnings for spray timing, but as reservoirs of biocontrol fungus. Further study is required.

And so Jonathan Swift’s observation rings true: “…a Flea/ Hath smaller Fleas that on him prey,/ And these have smaller yet to bite ’em,/ And so proceed ad infinitum…”. Powdery mildew will always be around, but for Ampelomyces that’s a good thing.

the vision thing

Research sponsored by the US Department of Agriculture has made progress since the old days.  The original model was for agricultural scientists to do research on field stations for the purpose of improving yields, and then hold up the results to farmers as the best methods for farming.  However, when the new methods met the off-station environmental conditions and social and economic constraints, they didn’t always perform well.  Nowadays the USDA, through its funding arm the National Institute of Food and Agriculture, mandates on-farm research and collaboration with relevant parties.  In this way the research gains relevance in real-world situations.

 

What might this arrangement mean for sustainability?  Consider the NIFA program known as the Agriculture and Food Research Initiative.  AFRI offers a grant with the title of Sustainable Agricultural Systems to fund efforts to increase production while keeping the environmental footprint of agriculture to a minimum, and it requires the involvement of a stakeholder advisory board in the management plan for any application.  The committees who review the applications check that the applicants have reached out to stakeholders, listened to their input, and molded the research plan to respond to their concerns.  The intended result is research that better addresses real-world issues of sustainability.  I always wondered, though, what if one of the stakeholders is a powerful interest, one that can take advantage of the rules of the process to marginalize the voices of small farmers, workers, academics, and environmentalists?  Depending on how the rules are set up, it is conceivable that the funded research could end up supporting the status quo over more sustainable alternatives.  Now there is some support for my suspicions — a team of researchers led by Jason Konefal out of Sam Houston State University in Texas presents a look into the dark side of stakeholder involvement, in a recent paper in the journal Renewable Agriculture and Food Systems.

 

Konefal et al. looked not at USDA-funded research, but at three private initiatives to develop a certification system for sustainably grown products, along the lines of the existing system for organic certification standards.  As interest in sustainable agriculture grows and consumers start to seek sustainably produced food, different streams of thought come into contention over what is truly sustainable.  At its most basic level, “sustainable” refers to a system that will provide for future generations.  However, different interests have different points of view on the details.  Konefal et al. differentiate weak versus strong sustainability, in which the weak form is basically conventional agriculture cleaning up its operations and becoming more efficient, while the strong form seeks to nurture functioning ecosystems, not just for the benefits these ecosystems provide to agriculture, but also for their intrinsic value, and along the way to build community and equity as well.

 

The first of the three initiatives, called Farm to Market, was started by an environmental conflict resolution organization with a utilitarian vision of sustainability, where technology is substitutable for natural resources.  There was no formal process for recruiting stakeholders onto the standards committee, but rather existing networks were used, and it was largely conventional agriculture interests who fit with the vision and were chosen to serve.  The stakeholders on the committee are of the opinion that US agriculture has become steadily more sustainable over the decades thanks to crop breeding and management techniques that have wrung higher yields out of existing land and resources.  Their resulting standards include requirements such as land use efficiency, water use efficiency, and energy efficiency, all areas where conventional agriculture can earn high marks.  Under their standards, chemical-intensive monocropping could be certified sustainable.  The committee also discussed economic and labor standards, but none have been put forth, leaving their certification system firmly in the weak category.

 

The second initiative, the Stewardship Index for Specialty Crops (“specialty” referring to fruits and vegetables), was started by the Natural Resources Defense Council, the Western Growers Association, and SureHarvest, with a vision of farming efficiency, ecosystem integrity, equity for farmers, and worker and community well-being.  The rules of the standards committee organize the stakeholders into three bodies, one representing mainly growers, one mainly buyers, and one environmental and public interest groups.  There was no formal recruitment process, and the first two bodies became dominated by big players in the conventional agriculture and food system.  In order for a standard to be approved, a majority of the members in each of the three bodies had to vote in favor.  Thus, in spite of a vision of strong sustainability and a diverse membership, conventional agriculture stakeholders essentially had a veto over any new standards that would put their practices at a disadvantage, and the first set of standards that the initiative released promoted a vision of weak sustainability that focused solely on efficiency just as Farm to Market.

 

The third initiative, LEO-4000, was put together by the Leonardo Academy under strict guidelines of the American National Standards Institute.  Starting with a strong vision of sustainability, the Leonardo Academy released a public call for applicants to serve on the standards committee, and from a large pool of applicants it screened and selected a diverse set of stakeholders representing conventional agriculture, environmental groups, worker organizations, and others.  As this diverse assemblage began to hammer out initial principles, they fell into two opposing camps, one representing conventional agriculture and one representing environmental and worker organizations.  A series of early votes went narrowly against conventional agriculture, and thirteen conventional ag stakeholders walked out, leaving the Leonardo Academy to scramble to fill those seats.  The process was completed, and the final set of standards reflected the strong vision of sustainability, albeit with some concessions to conventional ag.  In effect though, in spite of the fact that conventional ag stakeholders lost control of the third initiative, they still have a veto.  Their representatives point out that it’s the market that makes a certification valuable, and if conventional ag doesn’t want to be constrained by the requirements of a strong sustainability certification, they will take their business elsewhere.

 

So a narrow vision will end up giving the advantage to conventional agriculture, and a poorly designed governance system will end up giving the advantage to conventional agriculture.  And while a broad vision with good governance will promote practices that support the best principles, a reliance on market-based implementation may make it moot.

 

Going back to NIFA, the aforementioned Sustainable Agricultural Systems grant of the AFRI operates under a weak definition of sustainability mandated by Congress, where natural resources are to be preserved for future exploitation rather than ecosystem functioning, and efficiency is paramount.  If you’ll excuse my reading between the lines, the program seeks to increase production in a glutted national market, drive down food prices to accompany the assumption of ever-stagnating consumer incomes, and export farm products under the fiction that US producers are in charge of providing what other countries are perfectly capable of growing themselves.  Other stated goals are to reduce inputs, tap ecosystem services, introduce new technologies and new products, and promote consumer acceptance.  Interested parties are invited to contact the program with their comments, but there are no formal guidelines for designating stakeholders.  Environmental and social justice organizations may be able to weigh in, but they will be haggling over methods, not the underlying assumptions and goals.

 

Then there is the bigger picture.  NIFA has several grant programs in addition to the Sustainable Agricultural Systems initiative.  Consider the Specialty Crops Research Initiative, a source of funding that also requires stakeholder involvement.  The SCRI starts with the weak vision of sustainability, but whereas the AFRI has no set definition of stakeholders, the SCRI actually specifies “industry stakeholders” in its application.  In essence, the vision of the SCRI is to address the obstacles interfering with corporate profits, and thus the function of the initiative is to shovel more money to the interests that already have plenty, the interests that should need the least government assistance.  Any proposed research under SCRI must get buy-in from industry before the application can be submitted.

 

My question is answered.  Stakeholders in NIFA-sponsored research projects are self-selected or mandated to be industry representatives.  The stakeholders operate under a narrow vision of sustainability.  Under such a system it is doubtful that the research will lead to a vision of sustainability where crop germplasm is used wisely to head off crop collapse, where the poor can have a diet rich in nutrient-dense superfoods, and where all farmers can step off the pesticide treadmill.  Konefal and colleagues suggest that a non-market approach will be necessary to overcome moneyed interests and progress toward a strong sustainability.  Might I offer that a research funding system made up of a broad grassroots movement that supports researchers committed to an all-encompassing vision of sustainability could be a start?  I wonder.

a crop is a weed

If you’ve ever looked out along the roadsides of Portland, Oregon, you surely have noticed what looks like a tall dandelion in blue. This is chicory. Maybe you know chicory for its role as a coffee flavoring or coffee substitute, where the roasted root provides a certain nuttiness with a certain tang. The chicory variety that is forced from a root in the dark to produce a white bud is known as Belgian endive. Leafy varieties of chicory are eaten as greens in various countries, from Italy to Brazil. In the US leafy chicory varieties are sometimes marketed as dandelion greens, but perhaps more commonly the red varieties are known as radicchio. So why is chicory growing as a weed on the roadside? Was Portland once a hub of chicory production, blanketed with fields of bitter greens? Did seeds from a wild variety of chicory contaminate a batch of crop seeds and then go crazy in the new environment? Or did a tame plant from someone’s garden mutate into an invasive nuisance? Where would you turn to find out?

If you’ve been following this blog, you’ve probably already guessed that the answer is in the DNA. Just as DNA can be used to infer human ancestry, it is also indispensable for disentangling the past migration routes of other organisms, from salmon to yeast. Dr. Tomáš Závada used DNA to shed light on the origin of weedy chicory in the US. However, while the study of the human genome has been a colossal global endeavor, the global importance of the chicory genome ranks alongside that of Chinese red sage. Dr. Závada and his team had to rely on leftover gene sequence data from a study of the sunflower family tree, leveraging these data by using a curious property of DNA, the microsatellite.

Recall that DNA is a molecule made up of a long string of basic building blocks that come in four types. These building blocks can be thought of as letters in a code that contains the blueprint for all the structures and process in an organism; scientists refer to them as A, C, G, and T. All the cells in the organism contain the same blueprint, which is faithfully copied with every cell division using a tool known as an enzyme. Well, mostly. Every so often the enzyme that copies DNA makes a mistake, about once for every ten million DNA letters copied. The cell has additional machinery for correcting errors after they are made, but with hundreds of millions of letters and countless numbers of copies, a few errors always escape correction, providing the basis for evolution.

One type of error is particularly easy to make during the process of copying, the type that takes place where the sequence of DNA letters gets repetitive. The replicating enzyme will come across a short sequence, say, “AAG”, that is repeated a few times in a row — AAGAAGAAGAAG — up to a couple dozen times. Here the enzyme basically loses its place and is prone to skip an AAG or add and extra AAG. This type of repetitive sequence is known as a Single Sequence Repeat or, more picturesquely, a microsatellite. Every time a mistake in copying it happens — or any other type of DNA copying mistake as well — that is a mutation, and a new lineage is created. But while other types of mutations are often used to tell different species apart, microsatellite mutations happen so frequently that they are useful to distinguish lineages within a species.

Dr. Závada searched the online sunflower family DNA database for published chicory DNA sequences and found a dozen of these microsatellite stretches. There is lab equipment that can detect small differences between the size of a microsatellite from one plant versus another version of the same microsatellite from another, indicating a different number of repeats, and by extension, different ancestors. In addition to microsatellites the team used a segment of DNA that indicates matrilineal descent. It turns out that the chlorophyll-containing bodies inside a plant cell — the chloroplasts — have their own DNA separate from the cell’s nucleus. Chloroplasts are not present in pollen, so chloroplast DNA is only inherited from the female parent, the plant that produces the seed. Thus chloroplast DNA sequence that is found in one plant and matches that of another plant on a separate continent indicates that seeds must have been carried from one continent to the other. With the microsatellite sizes and the chloroplast DNA sequences, the team was poised to connect North American chicory lineages to crop varieties and wild varieties in their native Eurasian range.

Weedy chicory is actually found in all 48 contiguous United States. The team, based out of UMass Boston, sampled chicory plants from around New England and also received samples from other states, from Virginia to California. From the Old World they sampled different edible varieties of chicory, some grown for the root and some for the leaves, and also more primitive varieties from all over Europe plus Iran. The analytical software churned through all the data, and what interesting results popped out.

That Portland roadside chicory? It seems to be descended from radicchio, those characteristic red streaks in the leaves having been lost as it adapted to its wild lifestyle. The Boston weedy chicory matches the genotype of Belgian endive. The Boulder, Colorado, roadside chicory shares genes mostly with the wild chicory from Iran. The chicory stands in Nevada and New Mexico seem to have developed new mutations as they adapted to the local conditions. And the weedy chicory growing around Thomas Jefferson’s Monticello may be partly descended from the radicchio seeds that Jefferson received from France in one of the first recorded introductions of chicory to North America.

So does weedy chicory descend from extensive fields planted in another century? Chicory is sometimes grown as a fodder crop for livestock, but the genetic data do not clearly show descendants of fodder crops, possibly due to inadequate sampling. Did weedy chicory find its way to some of its current locations as a contaminant of crop seed? This phenomenon was documented for grass and clover seed in 1920 and may have been the case in places like Boulder. And in Portland? Because radicchio seems more like a horticultural crop meant for human consumption, it was probably not originally a contaminant, and it seems unlikely it would be grown as a salad for livestock. That leaves the third conjecture, the garden mutant.

To be sure, chicory started out with certain advantages for living wild, such as high seed production, a system for avoiding inbreeding, toxicity to competitor plants, tolerance to a range of environments, and an even ability to grow differently under different conditions. And in general, domesticated plants thrive in disturbed soils. Add to that the many introductions of chicory into North America, giving it many more chances to take hold, as well as plenty of genetic diversity for adaptation. In addition, variegated radicchio turns out to be a hybrid between chicory and its close relative, endive, the extra genetic resources supplying it with even more wherewithal to face adversity.

So a nice little radicchio from someone’s plot in Portland dropped seeds that sprouted in disturbed areas nearby. Then, years of cross-fertilization and environmental selection got rid of useless traits like red streaks and amplified traits that increased overall hardiness, and a re-wilded chicory took its place as a roadside weed alongside sweet pea, St. John’s wort, the feral race of carrot known as Queen Anne’s Lace, and that bane of all Oregonians, the blackberry. And the moral of the story is — be careful of the plants you import, because today’s exotic import could become tomorrow’s weed.

tagging along with a carbon atom

As any student of soil science will tell you, soil is not just dirt under your feet. Soil is so multifunctional that there are soil health advocates who sound like they must belong to some soil fan club. Healthy soil nourishes plants, nourishes humans, fights disease, fights drought, fights flooding, and recently soil has taken on another role — fighting climate change. In the wake of the 2015 Paris Climate Agreement, André Leu, president of the International Federation of Organic Agriculture Movements, spoke excitedly about the prospects for reversing climate change. Not slowing ‒ reversing. In response to the gloomy prediction of continued global temperature rise from carbon dioxide already emitted into the atmosphere, Leu advocates building up the organic matter in the soil through more conscientious agricultural practices. He calculates that if adopted on a global scale, such practices could draw down enough carbon from the atmosphere to bring the carbon dioxide concentration to pre-industrial levels in just 57 years, possibly sooner. Soil organic matter, the stuff that darkens soil brown to black, the stuff that is the basis for plant nutrition, disease resistance, drought resistance, etc., etc., provides a service that was not even conceivable a few decades ago.

The question then becomes, how does one build soil organic matter? Organic farmers have been working on this issue from the beginning of the organic movement and have made incorporation of manure and plant residues one of their central practices for achieving this goal. However, what became apparent from the work of researchers like Dr. Hollis Waldon was that microbes would then break down the added organic matter and exhale it as carbon dioxide back into the atmosphere, leaving little to no accumulation of organic matter in the soil. This season’s organic amendments have to be replaced come next season.

One method that has succeeded in increasing organic matter is no-till farming. In no-till, the tillage is replaced by herbicides or organic practices to manage weeds, and herbicides or crimping to terminate cover crops, and thus quantities of plant residue are left on the field. Most importantly, when the soil is not opened up, the microbes are deprived of oxygen and are slow to make use of the fuel in the organic matter. How does the organic matter get into the soil? How much organic matter might be contributed by the roots versus the aboveground portions of the plant, its “shoot”? How long does this season’s organic matter last in the soil? Is there a way to figure out where the carbon from the plant ends up after the plant dies?

There is. Researchers can essentially mark the carbon in carbon dioxide, feed it into the plant’s leaves, and detect it in plant residue and the environment afterward. This is done using rare variants of carbon. A well known carbon variant is carbon fourteen, abbreviated 14C, the same type of carbon at the heart of radiocarbon dating. The number 14 signifies that it has fourteen neutrons in the nucleus rather than the usual twelve, and this makes it radioactive. In carefully controlled laboratory experiments a researcher can use chemical compounds made with radioactive 14C in biological systems to discern with high sensitivity how the compounds move and where they end up, using techniques for detecting radioactivity. For open field experiments, though, researchers take advantage of a lesser known carbon variant, 13C. Its thirteen neutrons make its nucleus stable, so it can be handled without so much as gloves.

The non-radioactive 13C atoms are detected using a machine known as the mass spectrometer. The researcher takes a sample and burns it to turn the carbon back into carbon dioxide. The mass spectrometer gives the carbon dioxide molecules a charge and then shoots them through a magnetic field, which makes them curve toward a detector as they pass. A sample’s carbon dioxide will always contain a mix of regular and 13C. The extra neutron makes 13C heavier than the regular carbon, and that causes a carbon dioxide molecule made from it to travel slightly farther along the detector than an ordinary carbon dioxide molecule. The researcher records the proportion of heavy versus regular carbon in the various samples, and then with the appropriate bookkeeping determines exactly how much of the carbon dioxide that was originally applied has ended up in the samples of interest.

Dr. Emily Austin fed carbon dioxide containing extra 13C into a rye cover crop and followed it into the soil organic matter. She addressed the question of whether it is roots or shoots that contribute to organic matter accumulation by giving the 13C-enriched carbon dioxide to half of her cover crop patches and leaving the others open to the atmosphere. At termination, when she cut down the shoots, she switched the 13C shoots with the untreated ones. At that point, any 13C that was in the soil from which the 13C shoots were removed could only have come from the roots, and any in the plain-air patches that received 13C shoots would have to be from those shoots.

And the answer is, soil organic matter comes mainly from the roots. After five months ‒ the end of the summer corn-growing season ‒ there was four times as much organic matter from the roots and from the carbon that they had given off into the soil around them than there was from the shoots, and after a year there was seven times. By comparison, at the time that the shoots were first cut the roots had 1/6 less carbon than the shoots.

This result is consistent with the idea that lack of oxygen slows the breakdown of organic matter. Chopped leaves and stems sitting on top of the soil in this no-till system are exposed to oxygen and get broken down quickly by microbes, while buried roots are relatively protected. There is more to the story, though. Dr. Kris Nichols and other researchers who specialize in the beneficial fungi that live in roots claim that these fungi fill the soil with a sticky protein known as glomalin and that this glomalin is the source of recalcitrant organic matter, the organic matter that is hard to break down. With 13C flowing into the rye roots and their associated fungal partners, Dr. Austin was in a position to look for evidence of this claim.

Dr. Austin further processed soil samples from the experiment and extracted organic matter that had differing degrees of protectedness ‒ the unprotected free bits, the stickier stuff tucked away inside tiny clumps of mineral particles, and the small metabolites that form an intimate coating on the clay particles. She also chloroform-fumigated soil samples to extract total microbial biomass, that is, all the living fungi and bacteria. She then shot all these organic matter extracts through the mass spectrometer. The story that emerged from this finer analysis is that only about 2/3 of the carbon atoms that move into the roots are retained to build root tissue. The other third are sent directly to the soil. Growing root tips release carbon-rich mucilage that feeds microbes and coats soil particles. Slender short-lived root hairs and threads of fungi work their way into tiny aggregates of soil particles where they are relatively protected and deposit their carbon. Soil microbes incorporate the carbon into their cells within hours, and these cells turn over rapidly and release the transformed carbon into the soil, further contributing to the clumping and the coating of the particles. The organic matter that coats the clay particles is protected from degradation by the way it is bound to the mineral surface, suggesting that while the protein glomalin may play a role in binding aggregates together, it is not the only source of persistent organic matter. The shoots can enter the same pathway of transformation, but only at a later stage of breakdown.

What does this mean in practical terms? Dr. Austin’s focus is the loss of organic matter from farmland when the leftover stalks and leaves of a corn crop are hauled off for bioenergy. If the shoots of the corn account for a small fraction of the organic matter that builds up in soil, then the removal of a major portion of them can be fully compensated using the cover crop. Dr. Amélie Gaudin investigates the feasibility of increasing soil organic matter in fields where the shoots are grazed by livestock. Glomalin researcher Dr. Nichols insists that every field should have something growing on it at all times. In fact, at the end of Dr. Austin’s project, after a second corn crop, the amount of 13C detectable in the soil from the original cover crop had fallen to a very low level, and the difference in the relative contributions of root and shoot were negligible. Cover crops have to be used every year in order to build up soil organic matter and sequester carbon out of the atmosphere over the long term.

If soil organic matter buildup can play such a key role in pulling carbon dioxide out of the atmosphere, climate activists sometimes ask how to convince farmers to take on such a burden. One incentive is direct government payments to farmers who switch to methods that capture carbon dioxide, such as California’s Healthy Soils Program. However, increasing soil organic matter is in the farmer’s self-interest. One of the functions of soil organic matter is to increase the soil’s water holding capacity, and another is to decrease its erodibility. These are exactly the advantages a farmer needs to face a future of harsher droughts and bigger storms. Soil organic matter not only fights climate change, it helps farmers weather its effects. Soil organic matter lives up to the hype. Time to join the club.

cultivating community

To the uninitiated, the term “urban farming” may seem like something of a contradiction. The typical image of a farm might include a tractor, long rows of crops, clouds of dust drifting past a rickety barn, while the image of an urban landscape is that of entombed earth under austere buildings and roads, with the occasional manicured park. The combined term may evoke a community garden, or perhaps a legacy parcel of land on the fringe that has not yet succumbed to the march of concrete. What is not obvious from the term urban farming is that it is as much a political act as a means of providing food.

The California EcoFarm Conference has in recent years begun increasing its commitment to equity with its convocation of a Diversity Advisory Group. In 2019 the Conference featured as a keynote speaker urban farmer Karen Washington of Rise and Root Farm in New York, and showcased as successful organic farmers Chanowk (pronounced can-oak) and Judith Yisrael of Yisrael Family Farm in Sacramento. In addition to their plenary talks, these invitees participated in workshops dealing with equity and urban farming.

Rise and Root Farm is in upstate New York, but Bronx resident Karen Washington also participated in the urban community garden movement starting in the 1980s. She set the scene for the history lesson by evoking neighborhoods where buildings had been bulldozed in the wake of white flight during New York City’s fiscal crisis of the 1970s. The resulting open spaces became magnets for trash, not from the residents but from outsiders who dumped their loads in the dark of night, including tires and even automobiles. It was the residents who undertook the cleanup of vacant properties, only to find an endless supply of trash poised to fill the void. The advent of the community gardens was first and foremost a means of holding space that residents had cleaned up.

Gardening, however, is a fraught subject among African-Americans in the northern states. The history of slavery and Jim Crow has tainted their view of working with the earth, and many turn their back on planting and weeding in order to feel that they have moved ahead. Ms. Washington turns that historically based aversion on its head by pointing out to the members of her community that before slavery Africans were farmers. The reason that Africans were so crucial to agriculture in the humid southern US was not that they were mere laborers, but that they had the knowledge to farm in such a climate. Africans had domesticated rice independently, using an indigenous African species, and American plantation owners had to learn rice production from the Africans over whom they claimed ownership. Africans brought seeds with them from the old world. African-American families passed on the knowledge of medicinal herbs down through the generations. Today African-American urban gardeners can tap into a source of pride by learning the deeper history that has been kept from them.

With gardens beautifying the neighborhoods of New York, the community members felt that they had done a service to their city. Mayor Rudolph Giuliani took notice, but not in a good way. Seeing the opportunity to turn a profit off the volunteer labor of poor and minority people, Giuliani moved to auction off the land underneath hundreds of community gardens throughout the city. Thanks to the organizing that underlay the community garden movement, communities from all five boroughs sprang into action with a campaign of resistance that culminated in a lawsuit by Attorney General Eliot Spitzer blocking the sale and transferring the gardens to the Parks Department. That battle was won. Nevertheless, capital continues to test new schemes to dispossess the people.

Chanowk Yisrael had the epiphany to leave his IT job and harness his love of gardening to empower his community in the ‘hood. Starting out as a family operation, the Yisraels did not have to disabuse their fellow African-Americans of the notion that growing food was slave labor. Instead, nature did the recruiting. As urban dwellers spent time in the refuge of the garden, their eyes opened wide, they breathed easier, and their doubts melted away. The Yisraels’ sleight of social alchemy was to make their small farm a multi-use space where residents would be pulled in by community events and would leave as allies.

And allies became crucial for the functioning of the farm. When the Yisraels set up a farm stand they learned that selling garden produce was illegal in Sacramento. With the community at their back they approached City Hall and got the ban lifted. When the Yisraels wanted to set up a community farmers market, they had the foresight to approach community leaders in order to insure buy-in by the community before the market ever opened.

The Yisraels had to confront another legacy of racism, one now identified as food apartheid. African-American neighborhoods suffer from a dearth of grocery stores with fresh produce, a result of decades of social engineering and disinvestment. In their place are liquor stores, fast food joints, and food pantries. These areas have previously been referred to as food deserts, but activists point out that this latter term has been co-opted by the fast food corporations, and ecologists complain that the term does a disservice to deserts. What it meant to the farmers was that the residents did not know how to deal with farm stand produce.

Judith Yisrael had faced one of these knowledge gaps when she married Chanowk and his garden — how to prepare the variety of produce. Through trial and error she persevered, and now she runs edible education classes for the community. A more insidious knowledge gap surfaced when the residents asked why they should pay for the produce. The food pantry model upon which they had become dependent had instilled in them the expectation that food was free. The Yisraels had to educate them on the true cost of producing food, as well as the importance of community self-sufficiency. Non-profits that use their resources to provide free food are making the choice to not fund actual community development. The Yisrael Family Farm by contrast uses its profits to re-invest in the community. The neighbors who buy from the Yisraels are not just consumers, but what Karen Washington would call co-producers.

The inclusion of an equity track at the mostly white EcoFarm Conference allowed for a discussion of the role of white allies. Beth Smoker of the Pesticide Action Network spoke from her experience as a white person supporting communities of color. Sympathetic white people become allies when they ask how they can be supportive rather than imposing their own ideas about how to proceed. They have to be prepared for some discomfort as their understandings are challenged. Being an ally is an action, not a state of mind, and an ally must go out of his or her way to amplify the voices of the oppressed, rather than leaving the targets of oppression to take on the entire battle themselves. Mr. Yisrael recommends that white people who want to be allies read the chapter dedicated to white allyship in Leah Penniman’s book Farming While Black. In the end, white activists cannot transform the food system on their own. They will need to make alliances with African-American, Latino, Asian-American, and Native American communities who are on the front lines of confronting the unsustainable system that profits corporations while exploiting people and the environment.

in sickness

We often treat disease as an exception, a departure from the ordinary state of things. Thanks to public health infrastructure such as sewage treatment, restaurant inspections, and ventilation standards, we live disease-free for long intervals and don’t spend our all waking moments bracing for the cough that could signal misery, isolation, or death. Public health officials admonish us to cover our cough, wash our hands, get vaccinated, in short, to alter our behavior for the active prevention of disease, which is a menace that is always with us. However, not every employer offers sick leave, not every public gathering place supplies tissues, and not every medicine cabinet is stocked with unexpired analgesic, measures that can suddenly become necessary when the the darker side of life inevitably arises.

The situation is similar for agricultural producers. They prepare the soil, select the varieties, do the planting, manage water and fertility, weed, harvest, market the product, pay the workers and the creditors, and more. It would be understandable for them to relegate thoughts of disease to the back of their mind, especially with diseases they have no firsthand experience with. Disease is a chance event, and growers often get lucky. However, they ignore disease prevention at their peril.

Professor Cassandra Swett is a plant pathologist who bemoans the inattention that agronomists give to plant disease. Among other endeavors, Dr. Swett has lent her expertise to the study of deficit irrigation, an emerging practice intended to address water scarcity. The idea is to reduce water inputs only low enough to slightly stress the plants, not to reduce yield. In theory, plants can compensate for a certain amount of environmental stress. However, Dr. Swett’s first question is always about plant disease, and she is quick to point out that stress can often exacerbate disease, or even trigger symptoms in apparently healthy plants. Before she began asking about deficit irrigation and disease, none of the deficit irrigation proponents had considered that question.

Many fruit crops produce better flavor when they receive less than plentiful water. Tomatoes are one example, and thus a logical choice for deficit irrigation trials. Dr. Swett found that at light levels of deficit the plants had more infection with the fungus Fusarium than they would have under conventional water management, while at a greater deficit they had less infection. This finding of an apparently paradoxical result is also reflected in work her lab did with greenhouse poinsettias, where deficit irrigation reduced populations of water molds, but wherever the water mold organism Pythium was present it caused more disease. These are just the initial explorations of disease dynamics under deficit irrigation, but without Dr. Swett’s contribution, agronomists might have made sweeping recommendations that would have saved some growers money while costing other growers in terms of yield.

Dr. Kamyar Aram is a scientist at the Foundation Plant Service of UC Davis, the facility charged with providing virus-free grapevine propagation material to the nurseries that growers depend on for their supply. As part of his public outreach, Dr. Aram receives calls from California growers when their vineyard is overcome with viruses, at a point when little can be done to save production. Dr. Aram laments that growers generally do not regularly scout for virus symptoms and rogue symptomatic vines, that is, rip out infected individuals before the infection can spread and interfere with yields across the entire vineyard, or in terms of the enterprise, let go of underperforming assets before they become toxic across a wider portion of the portfolio.

The grapevine viruses causing the biggest dent in California wine production are the Grapevine Leafroll-associated Virus strain 3 and the Grapevine Red Blotch-associated Virus (“GLRaV-3” and “GRBaV”, following to the conventions of virus nomenclature). Grapevine viruses are transmitted through grafting infected material onto a new plant or through feeding and dispersal by sucking insects, such as mealybugs for GLRaV-3 or the three-cornered alfalfa hopper for GRBaV. Different virus strains presumably arose from an ancestral virus by coevolving in the grapevine population of a locality. Coevolved grapevines may tolerate their local virus, but a globalized grape-growing industry has spread viruses from every part of the grapevine’s native range to all the major wine regions. Such a situation can lead to viral infection of naive vines, mixed infections where viruses have synergistic effects on their host, and trading of virulence genes to create souped-up viruses.

Once a grapevine gets infected with a virus, it stays infected with that virus until the end of its life. Yield can be reduced, sugar production is impaired, and wine quality suffers. Vineyards that catch the eye with stunning red foliage in the fall are showing off virus infection; the vines’ natural fall color is yellow.

Grapevine Leafroll-associated Virus strain 3 is originally from Israel. Some traveler decided it was more important to get his hands on a particular grapevine for his vineyard than to protect the wine industry of an entire region. With the recent invasion of the vine mealybug into California, GLRaV-3 has a more efficient means of transport to move from vineyard to vineyard. The presence of the vine mealybug means that if you are a grape grower, your neighbor’s infected vineyard has become your affair. If your neighbor rips out his infected vineyard and replants, mealybugs can reintroduce virus from his neighbors. And because vine mealybugs can hide out on grapevine roots in certain soil types, a grower’s own soil can be a source of future virus infection.

Dr. Aram posits that growers in the Lodi area of California could eliminate GLRaV-3 for good if they all ripped out their vineyards simultaneously and kept the region grapevine-free for a season, and then re-planted with clean material. As far-fetched as this scenario might sound, it has been done in New Zealand and South Africa. In the US the emphasis on individual prerogative over collective action, codified in the economic system, generally makes thoughts of region-wide cooperative efforts inconceivable. Business as usual insures that GLRaV-3 will continue to be a problem.

Other examples abound. Dr. Honour McCann reminds us that the New Zealand breeders who developed the golden kiwifruit did so without considering the bacterial disease known as Psa that was attacking green kiwifruit across Asia at the time. This oversight caused the disease to spread on susceptible vines into New Zealand, Australia, and Europe, where treatment options are limited, and in some cases amount to an IV bag pumping antibiotic into each vine. An example from my own experience is the way some small growers will buy seeds from the bulk bin at the grocery store for planting. They save money on the purchase price of the seeds, but they don’t realize that unlike commercial seeds for planting, seeds marketed as food are not required to be produced on disease-free soil, they do not receive hot water or other treatments to kill seedborne pathogens, nor are they tested for pathogens. These growers are risking not just this year’s yield, but also the health of the field they plant in.

What should be done? Plant disease is an integral part of agriculture. All people involved in the agricultural system, from germplasm prospectors to breeders to agronomists to seed producers to growers to laborers to consumers should take a moment to inquire about the plant diseases to watch out for in their practices. Asking about plant disease should be as routine as washing your hands. Plant pathologists are standing by to take your call. As the American Phytopathological Society’s popular T-shirt says, “Don’t get caught with your plants down!”

Phytophthora man

 

Recent Ph.D. graduate Tyler Bourret is a phytophthorologist to watch out for. In his nascent career Dr. Bourret has pushed the boundaries of knowledge about that peculiar group of organisms known as Phytophthora.

Once believed to be a type of fungus, Phytophthora is actually a fungal-like organism descended from algae, a member of a group of organisms known in the vernacular as the water molds. It forms a network of tiny threads like a fungus, but its cell wall is made of cellulose, the same material that makes up plant cell walls, where a true fungus would have a cell wall made of a different material known as chitin. From its waterborne ancestors Phytophtora has inherited a type of spore that propels itself through water using flagella. Furthermore, it is not susceptible to many of the usual fungicides.

The name Phytophthora comes from the Greek, meaning “plant destroyer”. Phytophthora blazed a path of destruction across Europe starting in 1845, when late blight disease, caused by the species dubbed Phytophthora infestans, destroyed potato crops in several northern countries, notably Ireland. P. infestans’ uncharacteristically airborne spores allowed it to spread widely to infect whole fields of potatoes. Nevertheless, while many plant pathologists consider P. infestans as the cause of the so-called Irish Potato Famine, such a reductionist disciplinary view ignores the role of the English overlords, who exported great quantities of food from Ireland while the common people starved.

Since that time scores of other Phytophthora species have been discovered. The pathogenic forms normally cause root rot in annual and perennial crops and in wild plants, unlike the whole-plant-infecting P. infestans. The swimming spores take advantage of water-saturated soil, which can be a result of overwatering, to find a banquet of roots. The non-pathogenic forms live in ponds and streams, where they colonize dead plant matter and are probably what you smell when you get a whiff of stagnant water. The most recent species to grab headlines is Phytophthora ramorum, “Phytopthora of the branches”, cause of sudden oak death. P. ramorum can live in streams, colonize California bay trees without causing symptoms except for burned leaf tips, and then from those leaf tips produce spores that get splashed or blown onto the trunks of susceptible trees, most notably tan oaks, where they produce massive deadly cankers.

Sudden oak death burst onto the scene seemingly out of nowhere. At the same time that it was found devastating California woodlands, it was ravaging the European nursery trade. Only years later was a diversity hotspot of P. ramorum was found in southeast Asia, indicating that region as its native range. Unfortunately this kind of knowledge gap is common regarding Phytophthora. Dr. Bourret and colleagues discovered new species of Phytophthora while monitoring streams for P. ramorum and also while screening native plants from a nursery that were used in a restoration planting. It is not known whether these new species are native or introduced because no coordinated effort has been made to survey Phytophthora in different habitats around the world.

The other gap in knowledge is the virulence of these species in introduced habitats. Phytophthora pluvialis, a North American stream dweller, is now causing epidemics on Monterey pine in New Zealand. Plants or soil coming into the US could carry a strain with the virulence capable of causing the next epidemic of forests or crops, and in an era of rollbacks of government spending and regulations, they may not be discovered before mass plant destruction. In another questionable endeavor, Dr. Soum Sanogo’s lab in New Mexico is experimenting with inoculating the non-pathogenic water-dweller Phytophthora riparia onto chili pepper plants to essentially vaccinate them against Phytophthora root rot. Dr. Bourret points out that every Phytophthora species has all the machinery in its genetic makeup for causing disease in plants, but that the water-dwellers are generally overburdened with this machinery, making them easy targets for the plant innate immune system. The risk is that a water-dweller could lose some of its burdening genes and become a pathogen, as seems to have happened with Phytophthora megasperma.

One of Dr. Bourret’s areas of special fascination is the complex family tree of Phytophthora and its relationship with another set of algae descendants, the downy mildews. Downy mildews are not plant destroyers, but rather parasites that can only survive while their host is living, a condition known as obligate biotrophy. Their spores, still encased in their spore-bearing structures, travel through air and land on leaves to infect. The name comes from the fluff that appears on the underside of leaves when their threadlike growths exit through the leaf stomate pores to send off more spores. Because they are intimately dependent on their host’s cellular processes, they are confined to the single host species that they have co-evolved with. They are divided into twenty different genera based on characteristics such as host type, spore color, and leaf-penetration organ.

Since the turn of the current century, advances in molecular genetics have led to the unexpected finding that downy mildews are actually descendants of Phytophthora. The question then became where the downy mildews fit within the family tree if obligate biotrophy is all but absent in Phytophthora. Dr. Bourret analyzed the sequences of six common genes in over 100 species, including all of the downy mildew genera. His big innovation was to include an unusual species of Phytophthora from nutsedge that exhibits obligate biotrophy and an unnamed New Zealand Phytophthora species that was found infecting leaves of the totara tree, a conifer. He was able to show that the those downy mildews that infect sunflower-family plants are descended from a common ancestor they share with the nutsedge-infecting Phytophthora, and that the downy mildews that infect grasses, mustard-family plants, and others such as spinach descended from a common ancestor they share with the New Zealand leaf-infecting Phytophthora. Of course, with all the evolutionary changes required for a family tree branch to lead to true obligate biotrophy, the branches that lead to powdery mildews stick way out from the main tree.

Another result that popped out of the data is that of the six genes studied, those genes contained within the nucleus indicated some different family relationships among the different species than did the genes maintained outside of the nucleus. This disagreement suggests that sometime in the past there were hybridizations between species, or perhaps some species picked up DNA from the environment. Good science leads to the next set of questions, and Dr. Bourret is on his way to a lifetime of discoveries.

the magic of monoculture

The usual agroecological practices for preventing soilborne disease are well known: crop rotation, addition of organic matter and compost, sanitation of tools and plant materials, promotion of good soil structure, prudent water management, use of resistant varieties. Add to that list an incongruous entry — continuous monoculture. When the same crop gets hammered by the same disease in the same field year after year, once in a while the disease will suddenly disappear for good. This is the phenomenon of suppressive soil, and Daniel Schlatter and colleagues recently summarized the latest research on it.

While continuous monocropping contravenes good agroecological management on many levels, the appearance of disease suppression actually does arise out of agroecological principles. What we call disease is really the interaction between a host, in this case a crop plant, and a pathogenic organism. And whenever an organism is present in a field, it is subject to ecological forces. A field that contains a large population of a single species, whether it be a plant, insect, or microbe, potentially presents a target for another organism. For a plant, the opportunistic organism could be an insect or a fungus. For a microbe responsible for a crop disease, the opportunist could be an antagonist — a sort of armed competitor — or even a hyperparasite.

To be sure, a certain amount of disease suppression can come from enrichment of soil organic matter. Schlatter et al. differentiate this phenomenon as general suppression, the suppression that prudent organic farmers enjoy, whereby most soilborne diseases can cause only the most minimal damage. The other kind of suppression, that which arises from monocropping, is designated as specific suppression, where a specific disease caused by a single organism is the only one affected. Specific suppression can often be introduced into a field by addition of a small amount of already-suppressive soil. In addition, specific suppression requires the continuing presence of the host crop. If the field is rotated to a different crop, the resistance subsides, and it takes a season or more to return when the host crop is re-planted.

General suppression is thought to operate based on high numbers and high diversity of microbes present in the soil. This kind of microbial community insures that organic compounds are quickly broken down and taken up. Among these compounds are the exudates that a root characteristically gives off as it extends through the soil. It is these exudates that trigger pathogens to begin their attack. If the exudates dissipate immediately after release, the root may essentially slip past the pathogens unnoticed.

Regarding specific suppression, the authors of the review examine the mechanisms by presenting three case studies highlighting a continuum of suppression, from completely specific to somewhere between specific and general. The first regards the disease known as take-all of wheat. This disease is caused by a fungus that severely rots the plant’s roots. Certain strains of bacteria suppress the disease, and all of these turn out to produce an antibiotic known by the acronym DAPG. When these strains reach high population levels, the take-all pathogen is completely incapacitated and the disease disappears. The wheat plant’s roots even exude compounds that promote colonization by the DAPG strains. However, the DAPG producers have no effect on other pathogens.

The second case is that of Rhizoctonia bare patch of wheat and sugar beets. There is evidence that the organisms antagonistic to the Rhizoctonia fungus possess a certain amount of cross-antagonism against other pathogens, but the bare-patch-suppressing microbes are the least well characterized of the three case studies.

The third case is that of potato scab, a disease caused by a strain of Streptomyces, a genus of bacteria perhaps better known as the source of the antibiotic streptomycin. Interestingly, the antagonistic organisms are also strains of Streptomyces. It seems that the potato plant’s exudates are a food source for a suite of highly similar organisms, and niche theory predicts that in such a situation the best competitor will win out. In this case, the various strains of Streptomyces boost their competitive abilities in the presence of this limited food source by producing unique antibiotics that kill off their competitors. A casualty of this antibiotic arms race is the strain that causes the scab disease.

This third case of specific suppression is the closest to general suppression, although the mechanism is different from the fast degradation hypothesis. The cocktail of antibiotics pulsing through the soil can serve to eliminate other pathogens besides the bacterial strain responsible for potato scab. In fact, disease-suppressive Streptomyces strains can sometimes be enriched in the soil by incorporation of certain organic amendments, such as rice bran or the mustard family plant wall rocket, the presumption being that a particular type of food will cause the microbes that are able to digest it to fight over it, launching their specialized chemical weaponry as the competition intensifies. Whichever management practice initiates the chemical warfare, once it starts, it may tilt the microbial community composition toward ever stronger competitors, leading to a self re-enforcing dynamic that in some cases leads to lasting suppressiveness even when the original crop or amendment is gone.

Disease suppression has long been a phenomenon that emerged from the black box that is the soil microbiome. New tools for microbiome research are beginning to shed light on the inner workings of that system, and Schlatter and colleagues enumerate some of the methodological considerations for further advances. They also call for additional studies that use the knowledge that has been gained about suppression mechanisms to further our understanding of the agroecological circumstances and the specific management practices that will enhance disease suppression. For instance, will tillage increase or decrease disease-suppressive Streptomyces? Co-author Linda Kinkel invokes niche theory in predicting that no-till might allow the different strains to begin to coexist and to ease up on the competition, while tillage would disrupt any coexistence dynamic and more likely set off a chemical arms race. Would that happen in the real world? In every situation? Only field research, with a boost from microbiomics, will give the answer. For the foreseeable future, though, continuous monoculture remains a questionable bet for sustainable agriculture.

Pierce’s Disease and the microbiome

As if you needed any more evidence that microbiomes matter, wife-and-husband team Caroline Roper and Philippe Rolshausen have given us a microbiome study around the phenomenon of grapevines that escape Pierce’s disease.

 

Winegrapes as a crop are uniquely susceptible to diseases due to their propagation method.  Existing grape varietals such as Cabernet Sauvignon, Chardonnay, and Zinfandel are relics from the eighteenth century or earlier, kept alive through cuttings that are grafted onto more robust rootstocks.  They cannot be bred for disease resistance due to consumer rejection of hybrid varietals.  In France it is even illegal to breed with traditional grape varietals.  Grapevine pathologists are thus always assured of a job.

 

Pierce’s disease is caused by the bacterium Xylella fastidiosa, the “hard-to-grow xylem vessel-dweller”, Xf for short.  The bacterium gets injected into the water-conducting vessels of grapevine and other hosts, where it forms a film on the inside of these microscopic channels.  It was thought that the bacteria build up to such high numbers there that they block the flow of water to the leaves and cause scorching.  However Hossein Gouran showed in his Ph.D. research that the bacteria in the film are not the life stage associated with the scorching.  Rather, it is the free-floating stage of the bacteria that induces the actual disease.  These cells that have broken free produce an enzyme that flows up the xylem vessels and attacks the cells in the leaves, causing the scorch symptoms.  This revelation is so new that Roper and Rolshausen do not acknowledge it in the introduction to their study.

 

Pierce’s disease has long been a minor nuisance in California’s grape-growing regions, showing up on field margins that are near streams.  The native sucking insect known as the blue-green sharpshooter picks up the bacterium in the wild streamside vegetation and then disperses into the nearby grapevines, where it feeds on green stems.  It inserts its mouthparts into the xylem vessels, where it injects the bacterium as part of its feeding behavior.  The leaves on that segment of stem are the ones that show symptoms, but after the leaves drop in the fall and the vine has undergone a chilling period, it can emerge pathogen-free in the spring.

 

If that were the end of the story, it would be a mere footnote in the litany of diseases of grapevine.  Now, though, the introduction of the much larger glassy-winged sharpshooter from the southeastern US into southern California has given the Xf bacterium the upper hand in that region’s grape industry.  The new insect can inject Xf into the woody tissue of the grapevine, causing a much more devastating infection, and it avoids wild vegetation, instead moving extensively through the region’s orchards and vineyards.  Entire vineyards fail because of Pierce’s disease, and in northern California grape-growing facilities one can find wanted posters showing hideous blowup photos of the glassy-winged sharpshooter.

 

The real footnote of this disease story is that in vineyards that are ravaged by Pierce’s disease, occasionally there will be a lone grapevine that has escaped the disease.  This surprise cannot be the result of genetic resistance because all the grapevines in the vineyard are clones of centuries-old varietals.  With microbiome research all the rage, Roper and Rolshausen and their research groups asked if there was something about the microbiome of the escaped vines that protects them from Xf.

 

Serious microbiome research has only become possible with the development of so-called “next-generation” DNA sequencing technologies, new methods of reading off millions of DNA sequences in parallel.  The sequence is the order of the four possible building blocks of DNA, strung together in long strands to form a code that a cell can read for its instructions.  Roper and Rolshausen used one such technology, the Illumina system, where the millions of DNA segments get anchored to a tiny surface for a microscopic light show.  Since a DNA strand is made up of two halves that fit together perfectly, when one half is removed it can be recreated based on the sequence of the other half.  By monitoring the construction of the missing portion, one can determine the sequence of both halves.  Every new DNA building block that the Illumina machine adds generates a tiny flash of light from each anchored segment, with a different color representing each of the four building block types.  The sequence of colors in the series of recorded images corresponds to the sequence of a DNA strand at a particular spot on the surface, and given the millions of sequences recorded, with some computation the entire sample’s DNA sequences can be characterized.

 

The Illumina technology is useful in microbiome work thanks to DNA barcoding.  There are a few genes that are universal, contributing to a microbe’s basic cell structure and functioning.  In particular, the genes for the ribosome are indispensable, comprising the main part of the machinery for reading the DNA code.  They vary hardly at all from microbe to microbe because the vast majority of possible changes would be lethal.  This consistency makes these genes easy to find in the jumble of DNA.  However, there are segments in the DNA of these genes that do not get used in the ribosome, and therefore are free to mutate without consequence.  Different mutations are carried by different lineages, and the resulting DNA sequences can allow a researcher to distinguish different groups of microbes.

 

Roper and Rolshausen extracted the sap from symptom-free vines in southern California vineyards ravaged by Pierce’s disease and in northern California hotspots of Pierce’s disease and used ribosome DNA barcodes to compare the sap microbial community to that of the sap from nearby vines that had succumbed.  They looked at both bacteria and fungi, and while some of the fungi they found were interesting, there were too few to pick out a consistent trend between symptomatic and asymptomatic vines.  The bacterial communities were indeed different, although not nearly as rich as the bacterial community of a soil or a human gut, and the researchers mentioned a lot of the bacterial groups found, using the Latin, for anyone who is interested.  The key finding was that asymptomatic vines were low in Xf but had a high level a certain bacterial strain called Pseudomonas, which is known to have biocontrol properties.  Is this the key factor allowing the vines to stay healthy?  More research is needed.

 

With a strain of bacteria able to protect grapevines from Pierce’s disease, conventional ag research’s aim would be to commercialize the strain, with the hope of allowing private laboratories to make a profit by providing vineyard owners with another specialized input.  The high-margin winegrape-growing corporations would in turn be able to increase profits by extracting higher yields from their centuries-old relics, while any artisanal grower without the means to inject all her vines with a specially formulated bacterial preparation would be economically disadvantaged.  By contrast, the aim of agroecological research would be to seek management techniques that any grower could use that would increase the resistance of the vines to Xf.  This would be in the context of promoting overall agroecosystem health and community benefit.  I would even surmise that if varietals bred for disease resistance were ever to find acceptance, it would be by wine club members dedicated to small agroecologically managed vineyards.  More agroecological research is needed.

resistance gene networks

Plant breeders face a conundrum when it comes to plant diseases. The most powerful disease resistance genes, if not managed well, will quickly become useless.

Plants have an innate immune system that recognizes certain molecules that are typically found on pathogens. When a microbe presenting a typical molecular signature enters a plant, the plant basically bleaches the area using highly reactive oxygen compounds. The plant then activates genes that insure the microbe will not spread. However, successful pathogens overcome the innate immune system using molecules called “effectors” that disable components of the plant’s detection or response system.

The story does not end there, though. Thanks to Darwinian evolution, plant populations can develop resistance to pathogens. A dramatic form of resistance is the so-called R gene, the major resistance gene. If a pathogen possessing a single potent effector arrives, it will run rampant in a population of its host species. However, natural plant populations are typically very diverse. Any individual plant that happens to have an R gene that matches the pathogen’s effector allows it to recognize the effector and turn on its so-called hypersensitive response. Microbes with effectors are considered so dangerous that the plant will go crazy bleaching the point of entry until all cells in the area, pathogen and host, are dead. The result is an inconspicuous dot of dead tissue that shows where a pathogen attempted penetration.

In a natural population, the plant with the R gene will outlive its susceptible neighbors and pass this gene on to its progeny. In agriculture, this type of gene is highly sought by breeders aiming to develop resistant crop lines. A field of plants with the R gene will stand firm against the onslaught of a pathogen, growing robustly and giving their full yield where susceptible plants would turn out stunted, discolored, deformed, or dead.

In a further turn of evolution, however, the pathogen population can include individuals with a novel effector gene that allows them to disable a plant’s R gene and carry out its invasion of the plant’s tissues. These individual pathogens will reproduce thousands of progeny that are able to infect all the resistant plants. The pathogen has broken through the resistance. This is a common event, as a pathogen’s lifestyle depends on infecting plants, and therefore it is built to evolve new effectors quickly.

Another type of resistance is partial resistance, termed QTL, for Quantitative Trait Loci. In this case, instead of a single gene in the plant that acts as a tripwire for the pathogen’s effector, the plant has various traits that make it harder for the pathogen to carry out its lifecycle. Perhaps the plant’s external surface is harder for the pathogen to traverse, or one of the plant’s targeted enzymes is only partially disabled, or the plant produces a metabolite that slows the pathogen’s growth. Any single gene for partial resistance buys the plant only a partial or temporary escape from the ravages of the disease, but if many of these genes are present in an individual, that individual can be as resistant to the pathogen as if it had the appropriate R gene.

As you can imagine, partial resistance genes are more work for plant breeders. The QTL-resistant crop varieties they release must have multiple genes bred into them, or “stacked”. There is an advantage, though, in that the odds of any pathogen individual having enough genetic mutations to overcome all the resistance genes is essentially zero. In fact, breeders could stack multiple R genes in the crop varieties they release as well and enjoy the same odds against breakthrough, but expediency often overrules prudence when disease threatens. Furthermore, if one breeder expends the time and resources to stack R genes while other breeders release varieties with single R genes, the pathogens may break through the single R genes one by one, and the crop line with the stacked R genes may end up with few or just one functioning resistance gene. In that case, the pathogen population may be only one mutation away from breaking through the stack.

Plant pathologists are thus perennially concerned about release of resistance genes in seeds to farmers, but releases are often out of the control of the plant pathology commmunity. The network structure of plant pathologists, breeders, non-profit germplasm repositories, agribusiness corporations, and farmers presents a complex adaptive system where each actor has its own incentives, all of whom interact to produce the dynamics of resistance gene diffusion across the globe, both prudent and expedient. Karen Garrett and her plant pathology and plant breeding colleagues have looked into these dynamics using an epidemiological approach, published recently in Phytopathology.

Garrett et al. examine network structure for four staple crops: cassava, potato, rice, and wheat. The result is four abstract diagrams, evocative respectively of a double spiderweb, the tentacles of a sea anemone, a time-lapse photo of flocks of birds taking flight, and spaghetti with cheese flowing off a plate, all with colorful circles and squares on the periphery and black ones in the center. The central black circles show the centrality of the non-profit International Agricultural Research Centers, the IARCs. The other colors are codes for the continents where the different actors are located. Arrays of black squares represent private multinational companies, clustered near the center for potato and wheat, less obtrusive for cassava and rice.

The dots and squares on the periphery are segregated by color, signifying a dearth of direct connectivity between continents or regions. In terms of resistance gene diffusion, this means that there is no easy way for resistance genes from one continent to be bred into another continent’s crop, potentially leaving some areas without optimum disease protection. However, from the perspective of pathogen evolution, it could be helpful to have different resistance gene profiles in different regions to reduce the likelihood of the emergence of a super-strain able to infect the entire world crop. Also, less movement of the plant material containing the resistance genes means less likelihood of bringing hitchhiking pests and pathogens to new regions.

The reason for the four diagrams’ different arrangements of black squares — representing the international-scale private breeders — is the privileged position of some of their non-profit counterparts, the IARCs. In the case of cassava, a staple in tropical Africa and Latin America, the entire network is small, making the lone black square look rather incongruous and with very few connections. Private corporations seek out crops with the largest markets, and cassava is not one of them. In the case of rice, the authors explain that the international centers have played such a dominant role in the development of major resistance genes toward bacterial blight and rice blast diseases that there has been little profit incentive for the entry of private companies into the network. On the opposite extreme is wheat, for which several multinational corporations have extensive germplasm collections and have highly connected black squares in the network diagram. For potato there are similarly black squares in a more central position, but a closer look also reveals a proliferation of red squares on one side of the abstract anemone, representing a large number of private interests in wealthy Europe.

The abstract diagrams and their underlying analysis is a work in progress. The idea is to provide insight into what-if questions, such as how resilient a network would be if a major hub should disappear, such as the recent abandonment of the seed collection at the International Center for Agricultural Research in the Dry Areas in Aleppo, Syria (the Center was reconstituted in Lebanon and Morocco with backup seeds from the Svalbard vault). This type of change in a network would be unfeasible to test in an experiment, but past performance of the existing networks in terms of R gene diffusion and lag times can provide insights into the robustness of the complex adaptive system, as well as whether the networks themselves can be shaped by institutions embedded within them, e.g. the IARCs.

An observation by the authors is that private breeders tend to weaken the structure of the overall network. Whereas non-profit breeders’ focus is on providing farmers with plant material containing resistance genes, and ideally getting feedback on their performance from the farmers, private breeders have an incentive to hoard crop germplasm resources and release only those resistance genes that will make them a profit. Because of pro-corporate intellectual property laws and the development of biotechnology and hybrid varieties, private breeders are proliferating. The authors point out that private breeders focusing on more profitable markets enjoy a funding advantage for research over the constrained resources of the international research centers, thus allowing them to more quickly coordinate the release of resistant material. Poorer farmers have derived some benefit in the past due to trickle-down effects of resources originally directed at richer farmers.

A response to the privatization trend is the rise of open-source breeding movements, but the authors are unable to evaluate the effect of these efforts on breeding networks. Another shortcoming of the analysis, and of the underlying networks themselves, is the emphasis on staple crops. Traditional agriculture depended on a dizzying diversity of crops that is hard to fathom from the perspective of modern agriculture. This diversity provided an economic resilience to farmers as well as environmental services that benefited the crop plants, both of which have been replaced in modern low-diversity agroecosystems by continuous subsidies, in forms that range from pesticide development to resistance-gene prospecting to famine relief. A research focus on a handful of crops has promoted this low diversity, to the detriment of not just the environment but also human diet. While a big-picture analysis of the diffusion of resistance genes is an improvement over uncoordinated efforts to fight local outbreaks or to make a profit, such analysis must also be viewed as a small piece of the overarching big picture that is agriculture.