In 2004 a watershed event occurred in organic viticulture that may prove to be similar in its effect on organic viticulture as was the effect of the now-legendary 1976 Paris tasting on California wines, in which California wines roundly trounced the favored French. The 2004 event(1) was a tasting carried out by wine professionals to compare wines from non-organic “conventionally” produced grapes to wines from vineyards managed via a type of organic management known as Biodynamic. There were ten pairs of wines, all pairs consisted of one Biodynamic-sourced and one conventional vineyard-sourced wine. All pairs were of comparable region, price, and variety and were rated by the judges as to “best of pair” status. The outcome of the blind tasting stunned many in the premium wine world – the Biodynamic-sourced wines were rated superior in eight of the ten pairs, one pair tied, and only one of the conventionally-sourced wines was rated superior.
Wines made from grapes produced in organic and Biodynamically managed vineyards (as distinct from “organic wine” or “Biodynamic wine”*) have come on strong in the wine world in just the last few years. Dozens of premium label vineyards, led by the French, have converted to Biodynamic and organic management. A 2005 tasting event in San Francisco of 75 wines from Biodynamic and organic vineyards was a showcase for some of these wines from around the world.
If wines from organically or Biodynamically produced grapes† are indeed superior to wines from conventionally managed vineyards (all other factors being equal), what might the physiological and biochemical basis for such a difference be? This article introduces some of the physiology and biochemistry relevant to wine and food quality as it relates to the crop management and ecology.
Plant defense makes for quality components of wines and foods
In the 1970s this author was part of a small but spirited group of students of agricultural science at University of California Davis who were determined to learn as much about organic farming as we could. Although we were swimming upstream, UCD agriculture faculty at the time being more interested in the “better living through chemistry” approach, we regularly invited farmers from the then tiny organic farming community to come and speak on campus.
In their talks to us every one of those organic farmers related how their crops had a “vitality” that conventionally sprayed and chemically fertilized crops didn’t have, and that organic crops were naturally resistant to most pests and diseases. The majority of the UC agricultural science faculty at that time at best dismissed these claims, just as they generally dismissed all things to do with organic farming, which at least one professor called “voodoo agriculture”, and often ridiculed the farmers’ views as a regression to “primitivism.”
Now however, it’s a different story, one that vindicates those pioneering organic farmers. The ability of plants, particularly organically managed plants, to induce a type of situation-responsive immunity to attack by diseases and pests, is known as systemic acquired resistance (SAR), in which defense compounds, mostly phenolics, are produced. SAR has become one of plant science’s hottest research topics.
SAR is induced by low to moderate levels of insect and pathogen attack, a typical scenario in organic crop systems, and it turns out that this response is enhanced when composts and compost teas are applied, another typical organic scenario. SAR can be shut down when pesticides are applied.
It also turns out that many of the phenolic defense compounds that are produced via SAR are beneficial to human health. The term “nutraceutical” has been applied to this class of compounds. Resveratrol, the heart-healthy antioxidant compound produced in red grapes, is an example of a plant defense compound.
Additionally, phenolic and flavonoid compounds, many produced in the plant’s SAR defense system, turn out to be principal components in the “symphony” of compounds that define high quality wines. Below I discuss these issues with respect to Biodynamic and organic farming, and how various practices affect SAR and therefore wine quality.
Organic and Biodynamic viticulture and wine
It is to the credit of the premium wine community (along with chefs and restaurateurs) that it is leading, by a couple of lengths, the North American food industry in recognizing the connection between ecological integrity of production and quality of product, and that a significant percentage of that community has recognized that organic production is a key to this quality. The author’s dissertation research benefited from the openness and far-sightedness of the California North Coast wine grape community, when two dozen vineyard owners/managers allowed me to collect data on how organically managed vineyards resist damage by the root-colonizing insect, phylloxera, significantly better than conventionally managed vineyards(2) (The damage is caused by soil-borne pathogenic fungi that invade the phylloxera feeding sites and rot the root. Organically managed vineyard soils have more of the protective beneficial microbes, plus systemic resistance probably played a part.)
Both Biodynamic and organic farming systems have clear guidelines and certification protocols – organic certification since 2001 overseen by the USDA National Organic Program regulations (3), and Biodynamics by the Demeter Association (4). This has made it much easier to compare wines and foods produced using the different systems, since the clear guidelines make for relatively easy categorization and analysis.
Biodynamics is considered by most to be a sub- or super-group of organics, sometimes described as organics plus a spiritual/cosmic element. All certified Biodynamic farms can be certified organic, and many have both certifications. In the US the total number of Biodynamic farms (all types) make up only about a percent or two of the total number of organic farms.
Founded on a series of lectures in Germany in 1924 by Austrian Renaissance man, Rudolf Steiner, who also created the Waldorf schooling system, Biodynamics predates organized organics by at least twenty years. Consisting primarily of a commitment to a spiritual-ecological connection to the farm and the organisms (including people) connected to it, Biodynamics has a number of very specific compost-making and crop husbandry practices, as well as practices for channeling cosmic or metaphysical forces for the well being of the farm and its organisms. The best known of these practices is a roster of eight compost preparations known as the 500-507 series, as well as the herbal infusions (teas) used on crops.
An element of humor, if not hilarity, has been injected into the California viticulture scene with the reaction of traditional on-the-ground vineyard managers to orders from on-high to convert vineyards to Biodynamic management and its “quirky” practices. Many, if not most, agricultural scientists and farm managers see Biodynamics and its doctrinaire practices as just that – quirky. However, blind tastings and consumer preferences are powerful forces for conversion.
Differences between organic and Biodynamic grapes and vine characteristics have been examined(5) by John Reganold, professor at Washington State University. Reganold’s work on northern California winegrapes, at a Bonterra vineyard, involved a 9-year replicated trial that compared organic vs. Biodynamic treatments. There were no significant differences between the two management regimes in nearly all field parameters, i.e. yield, soil nutrients, cluster characteristics, etc. The yield to pruning weight ratio, an important parameter for indicating vine balance and wine quality, was more optimal in the Biodynamic, and the Biodynamically treated winegrapes had significantly higher Brix as well as slightly higher total phenols and anthocyanins in the last year. The authors state that the soil at the experiment site had high fertility, and that differences between Biodynamic and other management regimes would be more likely to show up if the soils are of lower fertility.
These kinds of studies are needed to compare organic and conventional management, as well as integrations of the two systems, which, in my view, is the way of the future in agriculture. Europeans have done much more research that examines the integration of organic and conventional practices in agricultural research, a category known as “integrated”, which often comes out being the superior treatment when all parameters are examined – yield, product quality, environmental impact, and net returns. Winegrapes for high quality wines however, may be much more sensitive than other agricultural products to seemingly innocuous practices like the occasional spray, as we will see below.
One of the most important contributions of the organic farming movement, I believe, has been that horticultural practices that probably never would have been tried by the researchers and practitioners of non-organic agriculture are being adopted after they have proven to be cost-effective and efficacious by organic practitioners. Often this crossover comes from a conventional grower who has put 10% of his ground into organic production, just to hedge his bets and try it, who then learns that some of those organic practices work pretty well.
Vine systemic acquired resistance and wine phenolics
Phenolic compounds are considered to be the most important component of the winegrape for giving uniqueness and character to wines of the same variety and quality of production. Indeed, the expression of terroir in red wine is considered to be a function of its phenolic composition (6,7). Terroir is that gustatory and olfactory aspect of wines that reflects the land – especially the soil.
There are scores of different phenolics produced in grapes, many induced in the SAR process – flavonols such as quercetin, anthocyanins such as pelargonidin and delphinidin, benzoics like vanillin and gallin, cinnamics such as coumarin and caffein, flavan-3-ols such as catechin and gallocatechin to name just a few. Terpene aromatics such as citronellol, linalool, and geraniol, which can be important olfactory elements in wines, are also important phenolics. It is the composition and ratios of these compounds that give variation and uniqueness to premium wines.
Resveratrol, the compound in grape skins that has a number of beneficial health effects in humans, is not an incidental product in the plant – it is a phytoalexin defense compound and anti-oxidant, produced when induced by SAR as well as by ultra-violet light and perhaps other factors.
The biochemistry of plant SAR is enormously complex (the following summary based on 8,9,10,11) and is still being worked out in laboratories around the world. The SAR process starts with what is known as the hypersensitive response which is set off when a pathogen initially infects plant tissue. This consists of an “oxidative burst”, i.e. the production of reactive oxygen compounds, leading to localized cell death and isolation of the pathogen to prevent it from spreading. Hydrogen peroxide is an important compound in the hypersensitive response. Insect attack causes a similar reaction in the plant.
Immediately following the hypersensitive response, signals are sent through the plant (signal transduction in both plants and animals has been one of science’s hottest research topics) which cause changes in gene expression all over the plant. The result is the production of situation-specific defense compounds, mostly phenolics. The terms “systemic” and “induced” or “acquired” are therefore used, since the compounds are produced as part of a system that senses attack in one part of the plant and then induces defense compounds in as yet uninfected parts.
Some phenolics are only produced via SAR induction, others only via constitutive (hardwired, turned-on all the time, not situation-specific) channels, and some may be produced via both channels. SAR tends to have a high energy cost in the plant and can reduce growth and yield in situations where there is no attacker for the energy-expensive defense compounds to defend against. Thus, in plant evolution the selection pressure would be strong for situation-specific induction of defense-compound production – in other words, all other things being equal, plants that have situation-specific defenses would have higher fitness over plants that have defenses turned on all the time.
Two main metabolic pathways are involved in SAR, the salicylic acid pathway, generally induced by pathogens, and the jasmonic acid pathway, often induced by insect attack. Considerable “cross-talk” occurs between these two pathways – sometimes they are additive and synergistic, and other times salicylate activity suppresses the jasmonic acid pathway. It appears that different branches of these two pathways combine in different situations, making for a complex interplay. Complicating this is the induction of jasmonic-SAR, or really a priming or strengthening of SAR, by rhizosphere (surface of the root-dwelling) bacteria, composts, and certain bacterial isolates ‡ – relevant to our organic connection. Additionally, some insects induce SAR channels that are normally only induced by microbes.
Common to both the salicylic acid and jasmonic acid pathways, upstream of them, is the shikimic acid pathway, an offshoot of pre-Krebs cycle phospoenolpyruvate, and source of the majority of phenolics in the plant. One of the three aromatic (ring-structured) amino acids, phenylalanine, is an important intermediate here. In SAR, phenylalanine is diverted from protein synthesis by an enzyme, phenylalanine ammonialyase (PAL), which de-ammoniates the molecule and converts it to phenol precursor cinnamic acid. This becomes important below in the discussion of herbicide use.
A number of familiar intermediary compounds are involved in SAR, such as hydrogen peroxide, cinnamic and coumeric acids, and ethylene, not to mention salicylic acid.
Current scientific knowledge of the salicylic and jasmonic SAR pathways, their inducers, and their end products is more in the realm of “the more we find out, the more we realize we don’t know”. One inducer will elicit one pathway in one species and the other pathway in another species, while a different dose or different timing can change those outcomes. In some situations the application of an inducing compound will weaken a plant’s defenses against a given attacker because the applied elicitor induces the wrong pathway, which inhibits the desired one.
Viticulture effects on SAR
Despite the physiological complexity of SAR, a few facts and anecdotal tidbits can be filtered out of the scientific and other literature relevant to the hypothesis that organic or Biodynamic methods enhance SAR and subsequent defense compound production and eventually wine and food quality.
Organically produced fruits have been shown to be higher in phenolic compounds than comparable conventionally grown fruits12 13. The salicylic acid content of soups prepared from organically grown vegetables was shown in research from the UK to be nearly six times higher than comparable soups from conventionally grown vegetables14, an indication of the relative levels of SAR activity. Critics, in a typically narrowed reductionist view, advised taking a half an aspirin a day to make up for this. They were apparently unaware that salicylic acid is an upstream precursor of dozens of phenolic and other compounds that may be beneficial to human health, and that higher salicylic acid levels would be an indication that there are other defense compounds, unmeasured, in the soup.
The effects of agri-chemicals on the rhizosphere and phylloshpere (leaf surface) microbe community (including endophytic microbes that colonize intercellular space in the leaf) is not well known, and even less is known about how such chemicals affect the SAR-inducing and SAR-enhancing relationship between those microbes and the plant.
Agrichemicals can have a substantial effect on SAR. One of the most important findings, in my opinion in this arena comes from a research report that showed that grape berry resveratrol production in vines treated with fungicides was reduced by up to 70%15. This makes sense – if the attacking microbes are eliminated, the plant no longer needs to produce the defense compound. This is a good example of the plant’s ability to conserve resources by turning off SAR when not needed. This research only looked at resveratrol, and that other phenolic compounds may be affected as well.
It is interesting to note that the mode of action of glyphosate, the most widely used herbicide in agriculture, is to shut down the shikimic acid pathway, the main precursor to phenolics in the plant. It has been shown that crop lines that have been genetically modified for glyphosate-resistance are more susceptible to fungal pathogens due to the re-engineering of this important plant defense pathway 16,17. It is unknown, however, whether sub-symptomatic exposure of normal, non-engineered plants to glyphosate, such as grapevines in a vineyard situation, has any effect on the shikimic acid pathway and the production of phenolics.
The soil fertility regime can have effects on plant compounds relative to wine and food quality. Applications of soluble synthetic nitrogen fertilizer cause a different response in the plant than the daily small N release pattern typical of the thriving soil microbial communities in mature organic crop systems, and this can bring about significant changes in resistance to insect feeding as well as disease (reviewed in 18). High doses of soluble N have been shown to inhibit resveratrol production (op. cit. Fregoni). At least one Napa Valley premium winemaker maintains that conversion to organic fertility methods has eliminated the problem of stuck fermentations.
Composts and compost teas have been shown to induce SAR in studies at compost research pioneer Harry Hoitink’s Ohio State University lab19. Plants treated with compost-only showed SAR activity, as did plants subject to pathogen attack-only. However, the highest SAR activity was seen in plants that received compost and were additionally subject to pathogen attack, indicating a priming or synergizing effect of composts. Bacteria in the composts were shown to be the inducers, and the SAR effect disappeared upon compost sterilization. The authors state that a number of bacterial taxa commonly found in composts have been shown to induce SAR.
Many reports have shown that silica applications induce SAR and other defense mechanisms in plants20, protecting them, including grape21, from certain diseases. One of the Biodynamic compost preparations, 501 horn-silica, involves mixing tiny amounts of silica powder with manure, making an infusion of it, and applying it as a foliar spray. Whether such small amounts of silica could induce SAR is unknown. Another silica input in Biodynamics, though not as central a practice as the 500-series preparations, is the application of horsetail (Equisetum) tea for disease management. Horsetail is high in a biologically available form of silica. At least one vinifera winegrape grower in the viticulturally challenging humid eastern US uses horsetail tea for disease management (22). Many organic farmers swear by the application of rock dusts, which are mostly silica, to their crops, saying, among other things, that better color and taste are the result.
Hydrogen peroxide, a central compound in SAR, has a persistent “underground” following as a crop disease management tool in fertigation (irrigation water amended with fertilizers or other agri-compounds) water. This practice is not well documented, as it is non-proprietary§. Hydrogen peroxide, which is allowed in organic crop production, was used by at least one grower in my vineyard research roster as a tool to manage phylloxera damage caused by soil-borne pathogens. However, hydrogen peroxide use is risky because a little too much can damage the plant, due to its oxidative power, the very mechanism that it induces in the plant to kill pathogens.
A number of proprietary products are on the market that induce or modify SAR, often isolates of Bacillus, Pseudomanas, and other bacteria. One class of proteins known as harpins, produced by several species of plant pathogenic bacteria, induces jasmonic SAR. There are anecdotal accounts of better berry anthocyanin content and color as a result of the application of proprietary versions of harpin (Messenger(r)) to winegrapes (23). Benzothiadiazole (BTH), a synthetic functional analogue of salicylic acid in the plant, has been shown to increase production of resveratrol and anthocyanins in winegrapes, while at the same time increasing resistance to Botrytis cinerea (24).
The observation that Biodynamic viticulture enhances the expression of terroir in wine has been a comment made by a number of wine professionals (op. cit. Reilly). Quality and the expression of terroir in premium wine is essentially a function of the complex interplay of phenolics and other compounds – a symphony so to speak, influenced via SAR and its biotic and abiotic stimuli. The composition of those stimuli is unique to each environment: benign and pathogenic foliar microbes, insects, rhizosphere and other soil-borne microbes, soil type, solar radiation etc. Perhaps what vineyard managers need to do is become more like the orchestra conductor, coaching and conducting all of these different elements. This is precisely what Biodynamics is all about. As one Biodynamaic vineyard manager put it when talking about the founder of Biodynamic farming: “Rudolf Steiner saw the farmer as kind of like the conductor of an orchestra.”
Don Lotter has a Ph.D. in Agroecology from the University of California Davis, currently writes and teaches part-time based in Davis, and is looking at options for a career in sustainable agriculture. His email is firstname.lastname@example.org, website: www.donlotter.net.
* The term “organic wine” is not used in this article because wine labeled as “organic” must be made in accordance with the USDA organic regulation, which, among other things, prohibits added sulfites. A similar situation applies to “Biodynamic wine” and its certification. However, most premium winemakers, many of whom use organically-grown grapes, insist on adding some sulfites. Wine made this way from certified organically grown grapes can be labeled “made with organically grown grapes” but not “organic wine”. It is wines in this latter category, both Biodynamic and organic, that I am focusing on in this article. Note however, that in common parlance these wines are often called “organic wines.”
† Note: In this article, I may use the term “organic” to include Biodynamic, apologies to Biodynamic purists.
‡ This type of systemic resistance, which lacks a hypersensitive response, is known in most SAR-science circles as induced systemic resistance (ISR), as distinct from SAR. However, to keep things comprehensible to readers, I am using the term SAR for the entire plant systemic resistance milieu, including ISR.
§ Non-proprietary technologies and solutions are not being adequately researched. With the steady loss of public-sourced funding for research, a higher and higher proportion of agricultural research funding comes from the private sector and only targets proprietary (patentable) outcomes. Increasingly, university SAR researchers are looking to isolate genes and compounds for proprietary use, while research on non-proprietary techniques is increasingly being left to farmers, maverick researchers, and anecdotal reports. Non-proprietary techniques may be as or more efficacious than proprietary ones, and often the input costs are a fraction of that of proprietary inputs.
1 Reilly, J.K. 2004. Moonshine, Part 2. Fortune. 150(4): p.34.
2 Lotter, D.W. et al. 1999. Differences in grape phylloxera-related grapevine root damage in organically and conventionally managed vineyards in California. Hortscience, 34 (3):472-473.
5 Reeve, J.R., L. Carpenter-Boggs, J.P. Reganold, A.L. York, G. McGourty, and L.P. McCloskey. 2005. Soil and Winegrape Quality in Biodynamically and Organically Managed Vineyards Am. J. Enol. Vitic. 56(4).
6 Cheynier, V. et al. 1999. Phenolic composition as related to red wine flavor. In: Chemistry of Wine Flavor. A.L. Waterhouse and S.E. Ebeler (Eds.). American Chemical Society. Washington, DC.
7 Boulton, R.B. et al. Principles and Practices of Winemaking. Chapman & Hall, NY.
8 Bostock, R. 2005. Signal crosstalk and induced resistance: straddling the line between cost anad benefit. Annu. Rev. Phytopathol. 43: 14.1-14.36.
9 Durrant, W.E. anad X. Dong. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42: 185-209
10 Sticher, L. et al. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35: 235-70.
11 van Loon, L.C. et al. 1998. Systemic resistance induced by rhizoshere bacteria. Annu. Rev. Phytopathol. 36: 453-83.
12 Asami, D.K. et al. 2003. Comparison of the Total Phenolic and Ascorbic Acid Content of Freeze-Dried and Air-Dried Marionberry, Strawberry, and Corn Grown Using Conventional, Organic, and Sustainable Agricultural Practices. J. Agric. Food Chem. 51, 1237-1241
13 Alyson E. Mitchell, Alyson, Yun-Jeong Hong, Eunmi Koh, Diane M. Barrett, D. E. Bryant, R. Ford Denison,# and Stephen Kaffka 2007. Ten-Year Comparison of the Influence of Organic and Conventional Crop Management Practices on the Content of Flavonoids in Tomatoes. J. Agric. Food Chem., 55 (15), 6154 -6159, 2007.
14 Baxter, G.J. et al. 2001. Salicylic acid in soups prepared from organically and non-organically grown vegetables. Eur. J. Nutr. 40: 289-292
15 Smith, B.J. and J.B. Magee. 2002. Resveratrol content of muscadine berries is affected by disease control spray program. HortScience, 37(2):358-361.
16 Altman, J. and A.D. Rovira. 1989. Herbicide-pathogen interactions in soil-borne root diseases. Canadian J. Pl. Path. 11:166-172.
17 Liu, L. A.K. Punja and J.E. Rahe. 1997. Altered root exudation and suppression of induced lignification as mechanisms of predisposition by glyphosate of bean roots (Phaseolus vulgaris L.) to colonization by Pythium spp. Physiological and Molecular Plant Pathology. 51:111-127.
18 Lotter, D. W. 2003. Organic Agriculture. Journal of Sustainable Agriculture. 21(4): 59-128
19 Zhang, W.D. et al. 1998. Compost and compost water extract-induced systemic acquired resistance in cucumber and Arabidopsis. Phytopathology, 88 (5):450-455.
20 Epstein, E.E. 1999. Silicon. Annu. Rev. Plant Physiol. 50: 641-664
21 Bowen P.A. 1992. Soluble silicon sprays inhibit powdery mildew development on grape leaves. J. Am. Soc. Hortic. Sci. 17: 906-912
22 Figiel, R. Personal communication from Richard Figiel, Silver Thread Vinyards, Lodi, NY.
23 Matthiason, S. 2005. Personal communication.
24 Iriti M. et al. 2004. Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea. J Agric Food Chem. Jul 14;52(14):4406-13.