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

Abstract

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.

RESISTANCE EVALUATION OF MODERN RICE VARIETIES TO BROWN PLANTHOPPER Nilaparvata lugens STÅL

“…The adaptation capability of BPH was suggested caused by bacterial endosymbionts and yeasts that involved in insect nutrition. A wide range of endosymbionts had been associated with feeding capacity in BPH (Ferrater et al, 2015;Horgan et al, 2019). Resistant variety management is necessary and important to perform for extending effectiveness of the released varieties in the field (Horgan, 2018).…”

Changes in insecticide resistance and host range performance of planthoppers artificially selected to feed on resistant rice

“…Similarly, results from studies that examined differences in bacterial sysmbionts from the same virulent and avirulent planthopper populations have given inconsistent results (Tang et al, 2010; Wang et al, 2015; Xu et al, 2015). More recently, a study with green leafhoppers, Nephotettix virescens , has indicated consistent relations between abundance of the obligate symbiont Candida sulcus and virulence patterns following artificial selection (Horgan et al, 2019). A potential for endosymbiotic bacteria to determine planthopper virulence is noteworthy because of the role of bacteria in adaptation by insect herbivores to insecticidal proteins (Dowd and Shen, 1990; Dowd, 1992).…”

“…In recent years, considerable research attention has focused on the role of endosymbiotic microorganisms in virulence adaptation (Douglas, 1998, 2009; Noda et al, 2012; Ferrater et al, 2013; Hansen and Moran, 2014; Horgan et al, 2019). A number of studies have found that the densities of YLS in planthoppers vary depending on the nature of the plant host (vis-a-vis resistant or susceptible) and that densities change during selection for virulence.…”

“…Other possible determinants of virulence adaptation include changes to the composition or functions of endosymbiotic bacterial and yeast communities involved in insect nutrition. A wide range of endosymbionts has been associated with feeding capacity in planthoppers and other phloem feeding insects (Douglas, 1998, 2009; Noda et al, 2012; Ferrater et al, 2013; Hansen and Moran, 2014; Horgan et al, 2019). Monitoring of endosymbionts during artificial selection for planthopper virulence has indicated shifts in the abundance of yeast-like symbionts (Lu et al, 2004; Chen et al, 2011a; Ferrater et al, 2015; Horgan and Ferrater, 2017) and in key functional bacteria (Tang et al, 2010; Wang et al, 2015; Xu et al, 2015).…”

Adaptation by the Brown Planthopper to Resistant Rice: A Test of Female-Derived Virulence and the Role of Yeast-like Symbionts

“…Furthermore, the results of our experiments demonstrate that virulence adaptation can be partial because it involves several virulence mechanisms, it involves both the male and the female parent, and likely involves both the planthopper and its mutualist symbionts. Partial resistance is most pronounced during virulence adaptation in leafhoppers—for example, adaptations for leafhopper ( Nephotettix virescens (Distant)) nymphs to feed and develop on resistant rice can take as little as 5 generations, but adaptations to lay eggs on resistant varieties can take a further 10–15 generations of selection [ 45 ]. Our planthoppers also demonstrated partial adaptation to IR62 (they survived and developed well but were inefficient feeders and had slow population growth).…”