Saturated Very-Long-Chain Fatty Acids Promote Cotton Fiber and Arabidopsis Cell Elongation by Activating Ethylene Biosynthesis

Abstract

Fatty acids are essential for membrane biosynthesis in all organisms and serve as signaling molecules in many animals. Here, we found that saturated very-long-chain fatty acids (VLCFAs; C20:0 to C30:0) exogenously applied in ovule culture medium significantly promoted cotton (Gossypium hirsutum) fiber cell elongation, whereas acetochlor (2-chloro-N-[ethoxymethyl]-N-[2-ethyl-6-methyl-phenyl]-acetamide; ACE), which inhibits VLCFA biosynthesis, abolished fiber growth. This inhibition was overcome by lignoceric acid (C24:0). Elongating fibers contained significantly higher amounts of VLCFAs than those of wild-type or fuzzless-lintless mutant ovules. Ethylene nullified inhibition by ACE, whereas C24:0 was inactive in the presence of the ethylene biosynthesis inhibitor (l-[2-aminoethoxyvinyl]-glycine), indicating that VLCFAs may act upstream of ethylene. C24:0 induced a rapid and significant increase in ACO (for 1-aminocyclopropane-1-carboxylic acid oxidase) transcript levels that resulted in substantial ethylene production. C24:0 also promoted Ser palmitoyltransferase expression at a later stage, resulting in increased sphingolipid biosynthesis. Application of C24:0 not only stimulated Arabidopsis thaliana root cell growth but also complemented the cut1 phenotype. Transgenic expression of Gh KCS13/CER6, encoding the cotton 3-ketoacyl-CoA synthase, in the cut1 background produced similar results. Promotion of Arabidopsis stem elongation was accompanied by increased ACO transcript levels. Thus, VLCFAs may be involved in maximizing the extensibility of cotton fibers and multiple Arabidopsis cell types, possibly by activating ethylene biosynthesis.

The draft genome of a diploid cotton Gossypium raimondii

“…These results indicate that Sus, KCS and ACO are necessary for cotton fiber development, as was proposed in previous individual studies 2,3,29 . Also, the MYB and bHLH transcription factors preferentially expressed in fiber reported herein may be used to elucidate the molecular mechanisms governing fiber initiation and early cell growth.…”

“…Qualitative transcript differences in key fiber development genes 2,3,29 were found between the non-fibered G. raimondii and the fibered G. hirsutum species, as revealed by transcriptome (RNA sequencing, RNA-seq) analysis using samples extracted from cotton ovules 3 days post-anthesis (DPA). Of the four sucrose synthase (Sus) genes identified in the genome, three (SusB, Sus1 and SusD) were expressed at substantially higher levels in G. hirsutum than in G. raimondii (Fig.…”

Genome sequence of the cultivated cotton Gossypium arboreum

“…Ethylene is an important signaling molecule that promotes cotton fiber elongation in G. hirsutum 10,11,13 . Products of the 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) gene are involved in the last and rate-limiting step in ethylene biosynthesis during cotton fiber development 10,11 .…”

“…Products of the 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) gene are involved in the last and rate-limiting step in ethylene biosynthesis during cotton fiber development 10,11 . In G. raimondii ovules collected at 3 days postanthesis (dpa), the levels of ACO1 transcripts were ~1,000-fold higher and the levels of ACO3 transcripts were ~500-fold higher than in G. arboreum (Fig.…”

Transposable elements play an important role during cotton genome evolution and fiber cell development

“…Here we investigated TE distributions in the close vicinity of these identified gene loci. Figure 5A shows the genes that have TE insertion in upstream of coding sequence within the scope of ~5 kb and their roles in cotton fiber development based on previous reports (Huang et al, 2013;Han et al, 2013;Li et al, 2005;Wang et al, 2009;Shi et al, 2006;Qin et al, 2007;Qin et al, 2005;Li et al, 2013;Xu et al, 2009;Shan et al, 2014;Walford et al, 2011;Wang et al, 2013;Luo et al, 2007;Pei, 2015). We identified a copia-like retrotransposon insertion in the promoter region of a MYB-domain transcription factor only in the Dt subgenome that is positively correlated with its higher expression in the allotetraploid ( Figure 5B).…”