RNA editing fine-tunes transcriptional plasticity and enhances the adaptability of Myzus persicae to diverse host plants
Wenyuan YuiD, Jun WuiD, Rong HuiD, Zhimou LiniD, Peiyu YangiD, Zhichao HuiD, Pengshuai PengiD, Shuai ZhaniD, Jean‐Christophe SimoniD, Saskia A. HogenhoutiD, Gang WuiD, Shuangxia JiniD, Yazhou CheniD
Abstract
Parthenogenetic organisms can adapt to diverse and rapidly changing environments despite limited standing genetic variation, but the molecular mechanisms enabling such adaptability remain unclear. Here, we investigate this question in the green peach aphid (Myzus persicae, GPA), an asexual generalist herbivore capable of colonizing a wide range of host plants without underlying genetic change. By integrating RNA-seq and DNA-seq from genetically identical clones reared on different hosts, we identified 1,368 high-confidence RNA editing sites (RES), many of which exhibited strong host-dependent differences in editing levels. These RES encompassed all 12 possible nucleotide substitutions, with A-to-I, C-to-U, and U-to-C conversions being particularly prevalent. Editing at several sites shifted dynamically within 48 hours of host transfer and often coincided with changes in transcript abundance. Functional knockdown of the editing genes ADAR1 and ADAR2 reduced editing at specific sites, diminished fecundity, and abolished aphid survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical signatures of A-to-I editing are deeply conserved, the genomic locations and functional roles of edited transcripts are species specific, reflecting lineage-specific adaptive strategies. Together, our findings demonstrate that RNA editing provides a rapid, reversible mechanism for environmental acclimation in GPA, enabling adaptive phenotypic plasticity even in the absence of genetic variation. This work establishes RNA editing as a key molecular basis for the remarkable ecological generalism of clonal organisms. Significance statementA major question in evolutionary biology is how clonal organisms with little genetic variation rapidly adapt to diverse, changing environments. Here we show that RNA editing provides a mechanism enabling the parthenogenetic green peach aphid (Myzus persicae) to colonize a wide range of host plants. RNA editing generates transcriptomic diversity, responds quickly to host shifts, and is essential for adaptation, as silencing ADAR genes disrupts A-to-I editing, reduces fitness, and prevents survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical features of A-to-I editing are conserved, its genomic deployment and functional outcomes differ among species, reflecting lineage-specific strategies. These findings demonstrate that RNA editing creates a dynamic regulatory layer that offsets constraints of asexual reproduction.
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