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The Chen Laboratory

Genomics and Epigenetics of Polyploidy and Heterosis

Cotton Fiber

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Cotton is the world’s largest source of renewable textile fiber and a significant oilseed crop. Cotton fiber development undergoes rapid and dynamic changes in a single cell type, from fiber initiation, elongation, primary and secondary wall biosynthesis, to fiber maturation. Each cotton fiber is a single-celled seed trichome or hair, and over 20,000 fibers may develop semi-synchronously on each seed. The molecular basis for seed hair development is unknown but is likely to share many similarities with leaf trichome development in Arabidopsis.

The most widely cultivated Upland cotton (Gossypium hirsutum L., AADD) is an allotetraploid that arose in the New World between the A-genome like species Gossypium herbaceum L. (A1) and Gossypium arboreum L. (A2) and the D-genome like species Gossypium raimondii (D5) Ulbrich 1–2 million years ago. Notably, the A-genome species produce spinnable fibre (middle) and are cultivated on a limited scale, whereas fibre produced in D-genome species (left) is rudimentary and not useful.

Fiber phenotypes of the Upland cotton (G. hirsutum, AADD) (right) formed between extant progenitors G. aboreum (A2) (middle) and G. raimondii (D5) (left). 

Allotetraploid cotton produces more, longer, and stronger fiber (right), suggesting non-additive expression of homoeologous fibre-related genes, including GhMYB2A and GhMYB2D homoeologs in the tetraploid cotton. We show that GhMYB2D mRNA accumulates more than GhMYB2A during fibre initiation and is targeted by miR828 and miR858, generating trans-acting siRNAs (ta-siRNAs) in the TAS4 family. Overexpressing GhMYB2A but not GhMYB2D complements the gl1 phenotype. Mutating the miR828-binding site or replacing its downstream sequence in GhMYB2D abolishes ta-siRNA production and restores trichome development in gl1 mutants. Moreover, disrupting Dicer-like protein 4 or RDR6, the biogenesis genes for ta-siRNAs, in the gl1 GhMYB2D overexpressors restores trichome development. These data support a unique role for microRNAs in functional divergence between target homoeologous genes that are important for evolution and selection of morphological traits.

Gossypium hirsutum MYB2 (GhMYB2), a putative GL1 homolog, and its downstream gene, GhRDL1, were highly expressed during fiber cell initiation. Overexpressing both GhRDL1 and GhMYB2 in A. thaliana Col-0 try mutant plants produced seed hair in ∼10% of seeds as well as dense trichomes inside and outside siliques, suggesting synergistic effects of GhRDL1 and GhMYB2 with try on development of trichomes inside and outside of siliques and seed hair in Arabidopsis.

At the genome-wide level, we found enrichment of siRNAs in ovules and fibers during fiber development, whereas general repression of miRNAs in fibers correlates with upregulation of miRNA targets encoding transcription and phytohormone response factors, including the genes found to be highly expressed in cotton fibers. Rapid and dynamic changes in siRNAs and miRNAs may contribute to ovule and fiber development.

In plants, de novo CHH (H = A, T, or C) methylation depends on RNA-directed DNA methylation (RdDM) and CHROMOMETHYLASE2 (CMT2)-mediated pathways. We show dynamic roles of these two pathways in ovule and fiber development. RdDM-dependent CHH methylation is linked to gene activation in ovules, and additional CMT2-dependent methylation leads to silencing of transposons and nearby genes in fibers. Moreover, DNA methylation affects expression bias of homoeologous genes and fiber development. RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development. These findings provide novel insights into epigenetic regulation of organ development and polyploid evolution.

Five Selected Publications

  1. Pang, M., Woodward, A. W., Agarwal, V., Ha, M., Guan, X., Vanitharani Ramachandran, V., Chen, X., Triplett, B. A., Stelly, D. M., and Chen, Z. J. (2009) Genome-wide analysis revealed rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.) Genome Biology 10:R122.
  2. Guan X., Lee, J.J., Pang, M., Shi, X., Stelly, D.M., and Chen, Z.J. (2011) Activation of Arabidopsis seed hair development by cotton fiber-related genes. PLoS One 6(7): e21301.
  3. Guan, X., Pang, M., Nah, G., Shi, X., Ye, W., Stelly, D. M., and Chen, Z. J. (2014) miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nature Communications 5:3050.
  4. Guan, X., Song, Q., Chen, Z. J. (2014) Polyploidy and small RNA regulation of cotton fiber development. Trends in Plant Science 19:516-528.
  5. Song, Q., Guan, X., and Chen, Z. J. (2015) Dynamic roles for small RNAs and DNA methylation during ovule and fiber development in allotetraploid cotton. PLoS Genetics 11(12):e1005724.
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