Chapter 12
Chemical Communication Between the Parasitic Weed Striga and Its Crop Host A New Dimension in Allelochemistry
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Larry G. Butler Department of Biochemistry, Purdue University, West Lafayette, IN 47907
Adaptation of Striga to parasitism includes not only dependence upon a host plant for metabolic inputs such as water, minerals, and energy, but also for developmental signals. In this way parasite and host development are highly integrated. The early host-derived chemical signals Striga requires, for seed germination and for initiation of the haustorium by which it attaches to host roots, are exuded from host roots into the soil. After Striga penetrates the host root, subsequent developmental signals are apparently exchanged directly, through vascular tissue. Germination stimulants for most Striga hosts have been identified as strigol-type compounds (strigolactones). Sorghum genotypes which produce extremely low amounts of stimulant are resistant to Striga. The gene for this trait has been mapped and incorporated into improved sorghums being released for production. Subsequent host-derived signals required by Striga are being characterized for possible independent mechanisms of resistance.
Plants that have surrendered their independence and adopted a parasitic lifestyle generally obtain their water, minerals, and/or energy (in the form of photosynthate) from their host plant. But successful parasitism involves much more than dependence upon a host for metabolic inputs. In addition to these essentials, the parasite's growth, morphological development and even its manner of reproduction must be compatible with that of the host. In effect, the entire life cycle of the parasite must, to a significant extent, be integrated with that of the host. This integration is necessarily more intimate, more molecular, than the integration of plants which depend upon other organisms for pollination or seed dispersal with the lifestyles and characteristics of the organisms which provide these services. Because their requirements are so specific and complex, parasitic plants would seem to be more vulnerable than independent, non-parasitic plants. Successful plant parasitism involves a series of stringent conditions and interactions, all of which
0097-6156/95/0582-0158$08.00/0 © 1995 American Chemical Society In Allelopathy; Dakshini, K., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1994.
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Chemical Communication Between Parasitic Weed & Crop Host
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must be satisfied. These include, but are not limited to, recognition and selection of an available, compatible, competent host plant at the proper stage of development in an appropriate environment. Given these requirements, it is no wonder that parasitism is a relatively rare lifestyle among plants. Yet some parasitic plants are so successful that they have become serious agricultural pests. How do these parasitic weeds manage to satisfy these requirements? To answer this question is to invoke a truism: parasitic plants are exquisitely adapted to their hosts and to their environment. We are beginning to see, at least with one particularly troublesome group of parasitic weeds, the witchweeds (Striga species), that this adaptation to the host reaches down to the molecular level, with communication by means of stereospecific chemical signals, and that it may extend throughout the parasite's life cycle. Striga Biology and Life Cycle (7) The genus Striga in the family Scrophulariaceae is composed of some 50 species, all holoparasites of tropical cereals or legumes. Striga hermonthica (Del.) Benth and S. asiatica (L.) Kuntze are the species which cause the most economically significant damage to cereals. S. gesneroides (Willd.) Vatke is the species most serious on cowpeas and tobacco. These witchweeds constrain production of important food crops such as maize, millet, sorghum, and cowpeas, particularly in Africa but also in India. A severe infestation can result in complete loss of the crop, and to abandonment of otherwise productive fields. The Striga problem in Africa seems to be worsening, due to intensive cultivation involving continuous monocropping of host crops in an attempt to produce sufficient food for the burgeoning population. Unfortunately, many improved crop cultivars which have been introduced have proved to be highly susceptible to Striga. Striga seeds are minute (0.2 mm), numerous (up to 100,000 per Striga plant and up to 100 Striga plants per host plant), and long lived (there are reports of Striga seed viability up to 20 years). Their requirements for germination include a dormant after-ripening period of several months, then pre-conditioning in moist conditions for one to three weeks, and finally, exposure to a specific chemical signal produced by the host root. After germination, a second host-derived chemical signal induces the elongating radicle to differentiate into a specialized structure, the haustorium, by which the Striga seeding attaches to and penetrates the host root. Approximately half the Striga life cycle is subterranean, living completely parasitically on the host roots. Much of the damage to the host occurs at this phase, before the Striga plant emerges from the soil. The mechanisms by which the damage occurs are not completely defined, but diversion of host resources to the parasite accounts for only a small proportion of the damage. Once above ground, the Striga plant develops chlorophyll and becomes green (except for S. gesneroides), fixing some but not all of its own carbon. The flowers, which are purple, red, yellow or white depending upon the Striga species, develop rapidly and the numerous seeds are produced about the same time as those of the host crop. Comprehensive information on Striga characteristics, distribution, and control may be found in the volume edited by Musselman (7). Selective information
In Allelopathy; Dakshini, K., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1994.
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ALLELOPATHY: ORGANISMS, PROCESSES, AND APPLICATIONS
may be found in a research bulletin on crop breeding for enhanced resistance to Striga from Purdue University (2). Host Control of Striga Development by Means of Chemical Signals
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The first two stages of Striga development from seeds are controlled by chemical signals exuded into the soil around host roots. Germination. Once the after-ripening and pre-conditioning requirements are met, Striga seeds respond within as little as 3 hours after exposure to germination stimulant produced by the host root. The earliest detectable response is production of ethylene; radicle elongation is detectable by 10 hours (3). Although ethylene appears to be the ultimate germination stimulant within the Striga seed, the nature of the germination stimulant exuded by host roots, which triggers ethylene production, has long attracted attention. Sorgoleone. The first Striga germination stimulant isolated from a Striga host plant was a series of oily and unstable substituted hydrobenzoquinones (structure 1) collectively called sorgoleone, exuded as hydrophobic droplets from the tips of root hairs of sorghum (4,5). The low solubility in water of the active hydroquinones and their rapid oxidation to quinones, which are inactive as stimulants of Striga seed germination, suggested that only those Striga seeds close to the host root would be stimulated to germinate (6). This would be an advantage for Striga by leaving ungerminated and viable for another season those seeds too far away to reach the host roots. A more stable and mobile germination signal, capable of stimulating Striga seed germination farther from the host roots, would be less advantageous for Striga, because many more seeds would germinate and die, reducing the population of viable Striga seeds. OH
OH
Structure 1 Sorgoleone
The limited water solubility of sorgoleone and its ready oxidation with loss of stimulant activity are not consistent with previous studies of Striga germination stimulants collected from hydroponically grown host plants (7). The amount of sorgoleone produced by several sorghum genotypes does not correlate well with their susceptibility or resistance to Striga (8,9). Moreover, sorghum and other Striga hosts produce other germination stimulants, more stable and more water-soluble than sorgoleone, in widely varying amounts that do correlate well with susceptibility or resistance in several cases (8,10). We have concluded that sorgoleone plays only a minor role, if any, in controlling Striga germination (8). Sorgoleone, which has been synthesized (77), is a very active allelochemical, even in the oxidized (quinone) form which has no activity as a Striga germination
In Allelopathy; Dakshini, K., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1994.
12. BUTLER Chemical Communication Between Parasitic Weed & Crop Host stimulant. It is a selective natural herbicide (12,13) inhibiting electron flow in mitochondria (14) and chloroplasts (75), active at concentrations as low as those of rotenone (14). Sorgoleone at least partially accounts for weed-inhibiting allelochemical effects long reported for sorghum (75,76). It is a powerful contact allergen (72), as expected from its structure which is similar to that of urshiol, the active component of poison ivy. Strigolactones. The first naturally occurring Striga germination stimulant identified was the sesquiterpene derivative, strigol (structure 2). Strigol was originally isolated from root exudate of cotton (77), which is not a host for Striga, so the significance of strigol was long uncertain. The (+) enantiomer of strigol is active as a Striga seed germination stimulant at concentrations as low as 10" M (18), and concentrations as low as 10" M have been reported to be active (7).
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Strigol The key to the identity of the host root-derived compounds which apparently do control Striga germination, and to the significance of strigol, was provided by the identification of sorgolactone (structure 3), a close analog of strigol, as accounting for most of the Striga germination stimulant activity produced by sorghum roots growing in water (19). The same group of investigators also identified alectrol (structure 4), another close analog of strigol, as the major Striga gesneroides germination stimulant produced by cowpea roots (20). Our group here at Purdue University subsequently showed that strigol itself is the major Striga germination stimulant produced by maize and proso millet (but not pearl millet, a common Striga host)(27). In each case, these Striga hosts produce three or more strigol analogs with germination stimulant activity. Sorghum, for example, produces a small (
