Comparative Metabolomics Analysis Reveals Sterols and Sphingolipids Play a Role in Cotton Fiber Cell Initiation.

Qiaoling Wang,Li Huang,Fan Xu,Qian Meng,Ming Luo,Caixia Ma,Guiming Li,Qian Chen

doi:10.3390/ijms222111438

Qiaoling Wang, Li Huang + Show 6 more

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https://doi.org/10.3390/ijms222111438

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Abstract

Cotton fiber is a seed trichome that protrudes from the outer epidermis of cotton ovule on the day of anthesis (0 day past anthesis, 0 DPA). The initial number and timing of fiber cells are closely related to fiber yield and quality. However, the mechanism underlying fiber initiation is still unclear. Here, we detected and compared the contents and compositions of sphingolipids and sterols in 0 DPA ovules of Xuzhou142 lintless-fuzzless mutants (Xufl) and Xinxiangxiaoji lintless-fuzzless mutants (Xinfl) and upland cotton wild-type Xuzhou142 (XuFL). Nine classes of sphingolipids and sixty-six sphingolipid molecular species were detected in wild-type and mutants. Compared with the wild type, the contents of Sphingosine-1-phosphate (S1P), Sphingosine (Sph), Glucosylceramide (GluCer), and Glycosyl-inositol-phospho-ceramides (GIPC) were decreased in the mutants, while the contents of Ceramide (Cer) were increased. Detail, the contents of two Cer molecular species, d18:1/22:0 and d18:1/24:0, and two Phyto-Cer molecular species, t18:0/22:0 and t18:0/h22:1 were significantly increased, while the contents of all GluCer and GIPC molecular species were decreased. Consistent with this result, the expression levels of seven genes involved in GluCer and GIPC synthesis were decreased in the mutants. Furthermore, exogenous application of a specific inhibitor of GluCer synthase, PDMP (1-phenyl-2-decanoylamino-3-morpholino-1-propanol), in ovule culture system, significantly inhibited the initiation of cotton fiber cells. In addition, five sterols and four sterol esters were detected in wild-type and mutant ovules. Compared with the wild type, the contents of total sterol were not significantly changed. While the contents of stigmasterol and campesterol were significantly increased, the contents of cholesterol were significantly decreased, and the contents of total sterol esters were significantly increased. In particular, the contents of campesterol esters and stigmasterol esters increased significantly in the two mutants. Consistently, the expression levels of some sterol synthase genes and sterol ester synthase genes were also changed in the two mutants. These results suggested that sphingolipids and sterols might have some roles in the initiation of fiber cells. Our results provided a novel insight into the regulatory mechanism of fiber cell initiation.

Highlights

Cotton fiber is an extremely elongated single cell of seed epidermis and an important raw material for the textile industry
Exogenous application of a gluceramide synthesis inhibitor, PDMP (1-phenyl-2-decanoylamino-3-morpholino1-propanol), in ovule culture system obviously inhibited the initiation of cotton fiber, implying that the change of sphingolipids may be an important reason for the suppression of fiber initiation in two lintless-fuzzless mutants. These results suggest that sphingolipids and sterols may have some roles in the initiation of cotton fiber cells, which provides a novel insight for the further study of the regulatory mechanism of cotton fiber differentiation and initiation
The results showed that 9 classes of sphingolipids and 66 sphingolipid molecular species were detected in 0-DPA ovules, including PhytoSphingosine-1-phosphate (t-S1P), PhytoSphingosine (PhytoSph), Sphingosine (Sph), Ceramide (Cer), PhytoCeramide (PhytoCer), PhytoCeramides with hydroxylated fatty acyls (PhytoCer-OHFA), GlucosylCeramides(GluCer), Phyto-GlucosylCeramides (Phyto-GluCer), and Glycosyl-Inositol-Phospho-Ceramides (GIPC)

Summary

Introduction

Cotton fiber is an extremely elongated single cell of seed epidermis and an important raw material for the textile industry. The growth and development of fibers can be divided into four distinct and overlapping periods: initiation, elongation (primary cell wall formation), secondary cell wall (SCW) deposition, and maturation [1,2,3]. About 30% of the seed epidermal cells differentiate into spinnable fibers [5]. Elucidation of the mechanisms of fiber initiation is valuable to the cotton industry. In the past two decades, many genes involved in fiber cell initiation have been documented. Loguerico et al identified six MYB-related genes potentially involved in the differentiation and development of cotton seed trichomes by a PCR-based strategy. R2R3 MYB transcription factor GhMYB25-like has an important role in fiber initiation.

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