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.
Highlights
The phloem of grasses is consumed by a diversity of specialized insect herbivores
Six bacte‐ rial taxa, including the obligate symbiont Candidatus sulcia clade, showed abundance patterns that reflected the virulence of the leafhopper hosts on GRH2/GRH4‐PYL
These patterns were consistent during a second selection phase when their insect hosts were switched from T65 or GRH4‐near‐isogenic rice lines (NILs) to GRH2/GRH4‐PYL for six generations
Summary
The phloem of grasses is consumed by a diversity of specialized insect herbivores. rich in sugars and nutrients, phloem is deficient in several amino acids that are the necessary building blocks of insect proteins (Gündüz & Douglas, 2009; Wan et al, 2014). 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) 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, 2018). To relate potential changes in the microbiome to further adaptation, we continuously monitored the leafhopper col‐ onies for survival, weight gain, and egg laying throughout phase II selection We assessed their ability to damage the host plant as populations became increasingly virulent. We discuss our results in light of current knowledge of the microbiomes of insect herbivores and of the mechanisms of virulence adaptation in phloem‐feeding leafhoppers
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