Integrated miRNA and transcriptome profiling to explore the molecular determinism of convergent adaptation to corn in two lepidopteran pests of agriculture

Kiwoong Nam,Sylvie Gimenez,Emmanuelle D’Alençon,Philippe Audiot,Imène Seninet,Marion Orsucci,Nicolas Nègre,Réjane Streiff

doi:10.1186/s12864-021-07905-7

Abstract

BackgroundThe degree to which adaptation to same environment is determined by similar molecular mechanisms, is a topic of broad interest in evolutionary biology, as an indicator of evolutionary predictability. We wished to address if adaptation to the same host plant in phytophagous insects involved related gene expression patterns. We compared sRNA-Seq and RNA-Seq data between two pairs of taxa of Ostrinia and Spodoptera frugiperda sharing maize as host-plant. For the latter, we had previously carried out a reciprocal transplant experiment by feeding of the larvae of the Corn strain (Sf-C) and the Rice strain (Sf-R) on corn versus rice and characterized the mRNA and miRNA responses.ResultsFirst, we predicted the genes encoding miRNA in Ostrinia nubilalis (On) and O. scapulalis (Os). Respectively 67 and 65 known miRNA genes, as well as 196 and 190 novel ones were predicted with Os genome using sncRNAs extracted from whole larvae feeding on corn or mugwort. In On, a read counts analysis showed that 37 (55.22%) known miRNAs and 19 (9.84%) novel miRNAs were differentially expressed (DE) on mugwort compared to corn (in Os, 25 known miRs (38.46%) and 8 novel ones (4.34%)). Between species on corn, 8 (12.5%) known miRNAs and 8 (6.83%) novel ones were DE while only one novel miRNA showed expression variation between species on mugwort. Gene target prediction led to the identification of 2953 unique target genes in On and 2719 in Os, among which 11.6% (344) were DE when comparing species on corn. 1.8% (54) of On miR targets showed expression variation upon a change of host-plant.We found molecular changes matching convergent phenotype, i.e., a set of nine miRNAs that are regulated either according to the host-plant both in On and Sf-C or between them on the same plant, corn. Among DE miR target genes between taxa, 13.7% shared exactly the same annotation between the two pairs of taxa and had function related to insect host-plant interaction.ConclusionThere is some similarity in underlying genetic mechanisms of convergent evolution of two distant Lepidopteran species having adopted corn in their host range, highlighting possible adaptation genes.

Highlights

The degree to which adaptation to same environment is determined by similar molecular mechanisms, is a topic of broad interest in evolutionary biology, as an indicator of evolutionary predictability
There is some similarity in underlying genetic mechanisms of convergent evolution of two distant Lepidopteran species having adopted corn in their host range, highlighting possible adaptation genes
We showed that some microRNAs and their target genes were involved in phenotypic plasticity or adaptive evolution, this respectively by comparing either the molecular response of each strain on two host plants, or by comparing that of the two strains on the same host-plant [13, 17]

Summary

Introduction

The degree to which adaptation to same environment is determined by similar molecular mechanisms, is a topic of broad interest in evolutionary biology, as an indicator of evolutionary predictability. We compared sRNA-Seq and RNA-Seq data between two pairs of taxa of Ostrinia and Spodoptera frugiperda sharing maize as host-plant. For the latter, we had previously carried out a reciprocal transplant experiment by feeding of the larvae of the Corn strain (Sf-C) and the Rice strain (Sf-R) on corn versus rice and characterized the mRNA and miRNA responses. Populations have to keep their ability to survive and reproduce to be maintained upon environmental changes This is challenging especially when fast changes occur and require adoption of new features, either metabolic, developmental, behavioral, physiological or morphological providing an enhanced fitness, through the process of adaptation. In the case of adaptive evolution, populations can acquire a better fitted phenotype to the environment thanks to the spread in the population of pre-existing genetic variants or of new mutations conferring enhanced capability (For review, [2, 3])

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Conclusion