Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids.
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 (F(1) and F(7)) 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 F(1) but were stably maintained in F(7) 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 mid-parent 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.
Ha
Misook
M
Section of Molecular Cell and Developmental Biology, University of Texas, Austin, TX 78712, USA.
Lu
Jie
J
Tian
Lu
L
Ramachandran
Vanitharani
V
Kasschau
Kristin D
KD
Chapman
Elisabeth J
EJ
Carrington
James C
JC
Chen
Xuemei
X
Wang
Xiu-Jie
XJ
Chen
Z Jeffrey
ZJ
D017360:Arabidopsis / Q000235:genetics*; D001483:Base Sequence; D017124:Conserved Sequence; D044127:Epigenesis, Genetic; D018506:Gene Expression Regulation, Plant; D018745:Genome, Plant; D006823:Hybrid Vigor; D006824:Hybridization, Genetic; D035683:MicroRNAs / Q000235:genetics; D008957:Models, Genetic; D008969:Molecular Sequence Data; D011123:Polyploidy; D018749:RNA, Plant / Q000235:genetics*; D034741:RNA, Small Interfering / Q000235:genetics; D012689:Sequence Homology, Nucleic Acid; D013045:Species Specificity
D035683:MicroRNAs; D018749:RNA, Plant; D034741:RNA, Small Interfering