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Needed: New Paradigms for Weed Control Twelfth Australian Weeds Conference NEEDED: NEW PARADIGMS FOR WEED CONTROL Jonathan Gressel Plant Sciences, Weizmann Institute of Science, Rehovot, IL 76100, Israel Proverb: If you never change direction, you will end up where you are heading Abstract Weeds are the major pest constraint in ex- Molecular biology and biotechnology have much to tensive monoculture or near-monoculture agriculture, offer in upgrading biocontrol, but are hardly utilized as exemplified by the wheat-growing areas of Australia, in inoculum stabilization through to genetic engineer- where a weed such as annual ryegrass (Lolium rigidum ing of increased or decreased host range, increased Gaud) can evolve resistance to virtually every wheat- virulence, or for introducing failsafes. selective and many other herbicides. The evolutionary INTRODUCTION trends towards resistance may have been exacerbated by the penchant for rate cutting that facilitated new Weeds are and have been the major constraint to food types of multifactorial resistances, requiring new man- production in the world. Staying ahead of Malthus has agement models. Herbicide-resistant wheat can only intensified agriculture, increasing practices such as be helpful if the resistance is to a rarely used herbi- monoculture that are questionably sustainable. Sustain- cide, or one not prone to resistance problems, and/or able should be understood in the context of having the resistance is to more than one graminicide, for use in least possible ecological instability. As can be seen in resistance delaying mixtures. The likelihood of herbi- Australia, the evolution of the multiply herbicide re- cide resistant transgenes introgressing from wheat di- sistant biotypes of annual ryegrass is an extreme agonally into closely related grass species is quite low, agroecological perturbation, and current herbicide use and as those species are not weedy, the risk seems very patterns have proved to be unsustainable. long when evaluated with unbiased decision trees. The risk is somewhat higher for oilseed rapid introgressing Similar problems had been happening due to similar genes into related Brassica weeds, where there is a too practices around the world. The heavy use of great a risk. Tandem constructs of herbicide resistance monoculture, typically with the same herbicide regime, genes with “antiweediness” genes could alleviate prob- along with high harvest index, short stature, wimpy lems of introgression of resistance genes from crops (uncompetitive) crops has led to new weed problems. into related species without affecting the crop, e.g. tan- These are not annual or perennial weed problems, these dem constructs with genes that abolish secondary dor- are millennial weed problems. I include amongst them mancy, genes that abolish reactions to shading, or genes Echinochloa spp. in rice and other crops, as well as that prevent seed shattering. Such genes would remain the Striga species in sub-Sahara Africa that are para- tightly linked to the resistance genes. sitic on most crops, halving yields of 100M people (Berner 1995). I also include the grass weeds of wheats Biotechnology can assist weed control in wheat, and such as Lolium spp. around the world, and Phalaris in not just through the development of herbicide-resist- India, that are being mimicked by other grasses in their ant wheat. Modifications of the TAC-TIC (Transposons ability to evolve resistances to graminicides, and not with Armed Cassettes for Targeted Insect Control) necessarily according to mode of herbicide action. This paradigm for insect control using DT’s (deleterious unsustainable instability requires that we analyze why transposons) carrying kev genes (chemically-induced resistance evolved with such a vengeance, and to as- suicide genes) or other deleterious genes would facili- certain whether practices can be modified to delay evo- tate weed control without herbicides. Annual ryegrass lution. would be ideal to test this concept: multicopy transposons bearing desired traits transformed into We must also analyze what biotechnology might have ryegrass could be seeded in pastures. The transposons in store in herbicide-resistant crops and weed would quickly disseminate into indigenous ryegrass biocontrol, and adequately analyze the risks these tech- due to the obligate outcrossing of ryegrass, while not nologies might bring. If the risks of herbicide resist- affecting pastures, but would engender unfitness in ance moving from crops to related species is great, competition with wheat. failsafes should be designed and instituted instead of the two extremes proposed: banning biotechnology, and denigrating or ignoring the risks. Finally, it is posited 462 Twelfth Australian Weeds Conference that biotechnology can be used to reverse evolution; Spraying can be uneven, some weed seedlings are in e.g. to force weeds such as annual ryegrass to evolve the spray shadow of others, weeds such as ryegrass back from being a pernicious weed of wheat to being a often have a second flush of germination when much pasture grass that is not very competitive with wheat of the herbicide has dissipated. The underdosed indi- and disappears when wheat is grown. Some of these viduals are weakened by the amount of herbicide they technologies are unlikely to be developed by industry, receive. Any underdosed, weakened individual, bear- yet are in the long-term public good, and thus the pub- ing a mutation that bears even a small modicum of lic sector with widespread public support will have to survival value may survive and multiply. This muta- take a greater part in such developments. tion could slightly increase the rate the weed degrades the herbicide, could increase the level of herbicide tar- DOSE AND RESISTANCE get, or could slightly protect the weed against the toxic The economics of the extensive cultivation of some- products generated in a sick weed. Many such resist- what marginal agroecosystems in Australia have dic- ance systems are known and they can be governed by tated lowering input costs to the minimum. This has many types of genetic modification: point mutations resulted in the penchant for lowering herbicide rates that slightly modify herbicide binding or slightly in- of application to the bare minimum. Nowhere else are crease the Vmax of degrading enzymes; mutations in such low rates so widely used, which together with the promoters of the herbicide target enzyme or control- biology of annual ryegrass, to my mind explains the ling the levels of herbicide degradation; amplifications problems with that species. in the herbicide target gene; and/or the genes control- ling degradation. Such minor mutations are always When a cut rate that is just lethal to the population “positive” and are thus inherited in a semi-dominant (minimum dose lethal=MLD) is used in the field not manner. The first individuals with the slight modicum all the population gets that dose (Figure 1). of dominant resistance are heterozygous. They will cross with each other and the homozygous individuals with a double dose of the resistance conferring alleles will be selected for under the selection pressure of the low herbicide rate. Any individual bearing a further mutation will be even more viable and will cross with others. Thus, under low doses the mean LD50 for the population can slowly creep up due to this multifacto- rial mode of resistance, which was loosely termed poly- genic, as population changes are similar to those gov- erned by quantitative inheritance. A pioneering epidemiological study was performed by Figure 1. MLD (minimum lethal dose) in field condi- Ian Heap (1988) in Ron Knight’s lab in Adelaide just tions. Only higher doses provide the MLD to the whole after the first four cases of ryegrass resistance to population in the field, low doses provide the MLD to diclofop were discovered and initially characterized most individuals, Presumed distribution of diclofop on by brother John Heap (Heap and Knight 1982, 1986). annual ryegrass the field at 400, 750, 1200 g ae/ha, Ian Heap collected a large number of ryegrass seed illustrating the proportion of pests receiving each dose. samples from farmers who had used diclofop for dif- Double spraying is ignored, as are untouched escaped ferent periods of time. His data (Fig. 2c) have the typi- organisms (in ‘refuges’). Assumptions: each mutant cal scatter expected from field-derived materials col- gene dose provides protection for 50 g/ha beyond the lected from farmers with limited records on herbicide threshold of 200 g/ha. The cross-hatched area shows use history, but the pattern is clear as well as highly the sensitive population from which one gene dose will significant statistically: there is a creeping increase in be selected at low rates. Reprinted by permission of the mean level of resistance of whole populations that the American Chemical Society; from Gressel (1995) is a function of the number of seasons diclofop was used. This is seen by looking at the population slopes Unlike in the laboratory where precision equipment is that are indicative of mono-modal creep (Heap pers. used to spray synchronous weed populations, field dis- comm), and are not bimodal as intimated by Preston tributions are imperfect. Four-leaf plants are effectively and Roush (1998). This is illustrated schematically as underdosed when the MLD for three leaf plants. population shifts in Fig. 2D. 463 Twelfth Australian Weeds Conference Figure 2. “Sudden” appearance of major monogene resistance vs slow incremental creep of quantitatively inher- ited resistance. (A) Actual field data on resistance showing changes in weed populations in a monoculture maize treated annually with atrazine. Amaranthus retroflexus, Echinochloa crus-galli and Digitaria sanguinalis, the foremost weeds, were counted. The maize field was treated with atrazine from 1970 onwards (B). A population distribution description of the same data for Amaranthus in (A), where the relative dose rates (R/S) on the hori- zontal axis are arbitrarily plotted. (C) Slow incremental increase in the dose level of resistance in repeatedly treated Lolium populations. The line showing how the dose required for control may increase was drawn for demonstration purposes only.
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