Abstract:
Small RNAs, including microRNAs (miRNAs), small interfering RNAs
(siRNAs), and trans-acting siRNAs (tasiRNAs), control gene expression
and epigenetic regulation. Although the roles of miRNAs and
siRNAs have been extensively studied, their expression diversity
and evolution in closely related species and interspecific hybrids
are poorly understood. Here, we show comprehensive analyses of
miRNA expression and siRNA distributions in two closely related
species Arabidopsis thaliana and Arabidopsis arenosa, a natural
allotetraploid Arabidopsis suecica, and two resynthesized allotetraploid
lines (F1 and F7) derived from A. thaliana and A. arenosa.We
found that repeat- and transposon-associated siRNAs were highly
divergent between A. thaliana and A. arenosa. A. thaliana siRNA
populations underwent rapid changes in F1 but were stably maintained
in F7 and A. suecica. The correlation between siRNAs and
nonadditive gene expression in allopolyploids is insignificant. In
contrast, miRNA and tasiRNA sequences were conserved between
species, but their expression patterns were highly variable between
the allotetraploids and their progenitors. Many miRNAs
tested were nonadditively expressed (deviating from the midparent
value, MPV) in the allotetraploids and triggered unequal
degradation of A. thaliana or A. arenosa targets. The data suggest
that small RNAs produced during interspecific hybridization or
polyploidization serve as a buffer against the genomic shock in
interspecific hybrids and allopolyploids: Stable inheritance of repeat-
associated siRNAs maintains chromatin and genome stability,
whereas expression variation of miRNAs leads to changes in gene
expression, growth vigor, and adaptation.