Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance

Horgan, Finbarr G.; Bernal, Carmencita C.; Quan, Vu Minh; Almazan, Maria Liberty P.; Ramal, Angelee Fame; Yasui, Hirofumi; Fujita, Daisuke

doi:10.1016/j.cropro.2018.07.010

Cited by 7 publications

(22 citation statements)

References 49 publications

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“…Although the results from phase II were generally weak (only the results for Candidatus sulcia were statistically significant), nevertheless the patterns were consistent between both selection phases (I and II). Relatively weak responses during phase II selection may be due to the short selection period (six generations), which only allows partial adaptation to the novel host (Horgan et al, ; Rapusas & Heinrichs, ; Vu et al, ). Five of the endosymbiont taxa in particular ( Bosea , Candidatus sulcia , Dyella , Mycobacterium , and Sandaracinus ) showed strong responses to phase I selection and consistent response patterns from phase II selection.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

Section: Methodsmentioning

confidence: 99%

“…The colonies were each selected on the four rice lines (henceforth “natal” hosts) for 20 generations (5 populations × 4 natal hosts = 20 colonies). Details of selection and the nature of the selected colonies (their ability to develop on natal hosts) are described in detail by Horgan et al (). Briefly, selection was conducted as follows.…”

Section: Methodsmentioning

confidence: 99%

“…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, , ).…”

Section: Introductionmentioning

confidence: 99%

“…We assessed the microbiomes of these adapted colonies to identify possible microbiome associations with virulence of the insect host. Horgan et al () have also shown that N. virescens colonies successively reared on the monogenic resistant lines ( GRH2 ‐NIL and GRH4 ‐NIL) were capable of surviving and developing on the pyramided line GRH2/GRH4 ‐PYL without any prior exposure to that line (henceforth phase I selection). Therefore, we expected that aspects of microbiome community structure would be similar among colonies reared on GRH2 ‐NIL, GRH4 ‐NIL, and GRH2/GRH4 ‐PYL, but different from colonies reared on T65.…”

Section: Introductionmentioning

confidence: 99%

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

Horgan

Srinivasan

Crisol‐Martínez

et al. 2019

Ecology and Evolution

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The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We examined patterns in adaptation by the green leafhopper, Nephotettix virescens, to near‐isogenic rice lines (NILs) with one or two resistance genes and the recurrent parent T65, without resistance genes. Only the line with two resistance genes was effective in reducing leafhopper fitness. After 20 generations on the resistant line, selected leafhoppers attained similar survival, weight gain, and egg laying to leafhoppers that were continually reared on the susceptible recurrent parent, indicating that they had adapted to the resistant host. By sequencing the 16s rRNA gene, we described the microbiome of leafhoppers from colonies associated with five collection sites, and continually reared or switched between NILs. The microbiomes included 69–119 OTUs of which 44 occurred in ≥90% of samples. Of these, 14 OTUs were assigned to the obligate symbiont Candidatus sulcia clade. After 20 generations of selection, collection site had a greater effect than host plant on microbiome composition. Six bacteria genera, including C. sulcia, were associated with leafhopper virulence. However, there was significant within‐treatment, site‐related variability in the prevalence of these taxa such that the mechanisms underlying their association with virulence remain to be determined. Our results imply that these taxa are associated with leafhopper nutrition. Ours is the first study to describe microbiome diversity and composition in rice leafhoppers. We discuss our results in light of the multiple functions of herbivore microbiomes during virulence adaptation in insect herbivores.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Horgan

Srinivasan

Crisol‐Martínez

et al. 2019

Ecology and Evolution

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

Horgan

Almazan

Quan³

et al. 2019

Crop Protection

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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.

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Two decades of rice research in Indonesia and the Philippines: A systematic review and research agenda for the social sciences

Cuaton

Delina

2022

Humanit Soc Sci Commun

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While rice studies are abundant, they usually focus on macro-level rice production and yield data, genetic diversity, cultivar varieties, and agrotechnological innovations. Moreover, many of these studies are either region-wide or concentrated on countries in the Global North. Collecting, synthesizing, and analyzing the different themes and topic areas in rice research since the beginning of the 21st century, especially in the Global South, remain unaddressed areas. This study contributes to filling these research lacunae by systematically reviewing 2243 rice-related articles cumulatively written by more than 6000 authors and published in over 900 scientific journals. Using the PRISMA 2020 guidelines, this study screened and retrieved articles published from 2001 to 2021 on the various topics and questions surrounding rice research in Indonesia and the Philippines—two rice-producing and -consuming, as well as emerging economies in Southeast Asia. Using a combination of bibliometrics and quantitative content analysis, this paper discusses the productive, relevant, and influential rice scholars; key institutions, including affiliations, countries, and funders; important articles and journals; and knowledge hotspots in these two countries. It also discusses the contributions of the social sciences, highlights key gaps, and provides a research agenda across six interdisciplinary areas for future studies. This paper mainly argues that an interdisciplinary and comparative inquiry of potentially novel topic areas and research questions could deepen and widen scholarly interests beyond conventional natural science-informed rice research in Indonesia and the Philippines. Finally, this paper serves other researchers in their review of other crops in broader global agriculture.

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Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance

Cited by 7 publications

References 49 publications

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

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

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

Two decades of rice research in Indonesia and the Philippines: A systematic review and research agenda for the social sciences

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