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

Abstract

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.

Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines

“…We obtained DV85 and T65 from the Germplasm Bank at the International Rice Research Institute (IRRI) in the Philippines. The resistant lines that we used, GRH2 ‐NIL, GRH4 ‐NIL, and GRH2/GRH4 ‐PYL, were BC 6 F 5 generations selected using Simple Sequence Repeat markers associated with the target loci during repeated backcrossing of the donor variety DV85 and the recurrent parent T65 (Horgan et al, , ). Seeds of the NILs were bulked‐up in a screen‐house at IRRI during the dry season when temperatures were coolest.…”

“…These factors make it difficult to relate changes in microbiomes to the selection potential of specific resistance genes. Recently, a number of research teams have developed near‐isogenic rice lines that share common recurrent parents, but differ by containing specific gene loci introgressed through marker‐assisted selection from different resistance donors (Fujita et al, ; and see Horgan et al, ). By using such near‐isogenic lines, studies of virulence adaptation can better associate changes in microbiomes with the effects of specific resistance genes without confounding background genetic effects (Horgan, ).…”

“…Beginning in the 1970s, a number of studies indicated that leafhopper populations are variously affected by resistance factors present in traditional rice varieties (Fujita et al, ). Although the mechanisms remain largely undetermined, these resistance factors reduce leafhopper feeding, nymph development, and egg laying (Asano et al, ; Horgan et al, ). Currently, more than 24 loci with genes for resistance to leafhoppers ( Nephotettix spp.…”

“…Furthermore, genes associated with the production of volatiles, particularly sesquiterpenes, were upregulated during N. cincticeps attack (Asano et al, ). Previous studies have indicated that the pyramided line, GRH2/GRH4 ‐PYL, is highly resistant to N. virescens (Horgan et al, , ).…”

“…These factors make it difficult to relate changes in microbiomes to the selection potential of specific resistance genes. Recently, a number of research teams have developed near-isogenic rice lines that share common recurrent parents, but differ by containing specific gene loci introgressed through marker-assisted selection from different resistance donors (Fujita et al, 2013; and see Horgan et al, 2019).…”