Unanticipated benefits and potential ecological costs associated with pyramiding leafhopper resistance loci in rice

We tested the hypotheses that increasing the number of anti-herbivore resistance loci in crop plants will increase resistance strength, increase the spectrum of resistance (the number of species affected), and increase resistance stability. We further examined the potential ecological costs of pyramiding resistance under benign environments. In our experiments, we used 14 near-isogenic rice lines with zero (T65: recurrent parent), one, two or three resistance loci introgressed through marker-assisted selection. Lines with two or more loci that were originally bred for resistance to the green rice leafhopper, Nephotettix cincticeps, significantly reduced egg-laying by the green leafhopper, N. virescens. Declines in egg-number and in nymph weight were correlated with the numbers of resistance loci in the rice lines. To test the spectrum of resistance, we challenged the lines with a range of phloem feeders including the zig-zag leafhopper, Recilia dorsalis, brown planthopper, Nilaparvata lugens, and whitebacked planthopper, Sogatella furcifera. There was an increase in the number of tested species showing significant declines in egg-laying and nymph survival on lines with increasing numbers of loci. In a screen house trial that varied rates of nitrogenous fertilizer, a line with three loci had stable resistance against the green leafhopper and the grain yields of infested plants were maintained or increased (overcompensation). Under benign conditions, plant growth and grain yields declined with increasing numbers of resistance loci. However, under field conditions with natural exposure to herbivores, there were no significant differences in final yields. Our results clearly indicate the benefits, including unanticipated benefits such as providing resistance against multiple herbivore species, of pyramiding anti-herbivore resistance genes/loci in crop plants. We discuss our results as part of a review of existing research on pyramided resistance against leafhoppers and planthoppers in rice. We suggest that potential ecological costs may be overcome by the careful selection of gene combinations for pyramiding, avoidance of high (potentially redundant) loci numbers, and introgression of loci into robust plant types such as hybrid rice varieties.