Multi-omics dissection of transgressive expressed mechanism to reveal fiber yield heterosis in cotton (Gossypium hirsutum)

Hybrid cotton has great potential to improve fiber yield. Nevertheless, the genetic and epigenetic molecular mechanism underlying cotton heterosis remains elusive. To gain insights into these mechanisms, we conducted comparative transcriptomic and epigenetic analysis of two crosses (B985S and Z41S). The lint yield (LY) of Z41S was similar with the higher value parent while the LY of B985S was significantly lower than the higher value parent. Comparative transcriptomic analyses revealed that non-additively expressed gene number were extremely different in two tissues of two hybrids. In particular, 10,792 genes (14.66 %) in Z41S were non-additively expressed, and this percentage was significantly higher than those in ovule of Z41S and fiber and ovule in B985S. Furthermore, 78.06 % of the non-additively expressed genes showed transgressive expression in hybrid Z41S. This result indicated that transgressive expression maybe the major contributor to heterosis of Z41S. We further found that most of differentially methylated genes overlapped with non-additively expressed genes and genes which involved in the RNA-directed DNA methylation and de novo methylation pathway. The percentage of transchromosomal methylation and transchromosomal demethylation regions in CHH methylated sites of Z41S fiber was higher than other tissues. This result suggesting that non-additively expressed genes which exhibited demethylation in the CHH type play essential role for heterosis in hybrid cotton. Our results also suggested that 24-nt siRNA are important for CHH methylation level increase in cotton hybrids. A large portion of non-additively expressed miRNAs were transgressive expressed in hybrids, and most of target genes in hybrid Z41S showed non-additive expression patterns. Our multi-omics approach provides valuable clues into the genetic and epigenetic basis of cotton heterosis and opening new avenues for genetic manipulation and crop improvement. • Hybrid cotton has great potential to improve fiber yield. • Over 78.06 % of the non-additive expressed genes showed transgressive expression in Z41S. • Most of differentially methylated genes were overlapped with non-additive expressed genes. • 24-nt siRNA are important for CHH methylation level increasment in cotton hybrids. • Most of target genes of non-additively expressed miRNAs in hybrid Z41S showed non-additive expression.