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Blocked synthesis of sporopollenin and jasmonic acid leads to pollen wall defects and anther indehiscence in genic male sterile wheat line 4110S at high temperatures

  • Xuetong Yang
  • Jiali Ye
  • Lingli Zhang
  • Xiyue SongEmail author
Original Article

Abstract

Environment-sensitive genic male sterility is a valid tool for hybrid production and hybrid breeding, but there are no previous reports of the molecular mechanism of fertility conversion. In this study, RNA-seq, phenotypic and cytological observations, and physiological indexes were applied to analyze thermo-sensitive genic male sterility line 4110S under different temperature conditions to explore the fertility transformation mechanism. In total, 3420 differentially expressed genes (DEGs) were identified comprising 2331 upregulated genes and 1089 downregulated genes. The DEGs were apparently distributed among 54 Gene Ontology functional groups. The phenylpropanoid, long-chain fatty acid, and jasmonic acid (JA) biosynthesis pathways were related to male sterility, where their downregulation blocked the synthesis of sporopollenin and JA. Phenotypic and cytological analyses showed that pollen wall defects and anther indehiscence at high temperatures induced sterility. Moreover, enzyme-linked immunosorbent assay results indicated that the abundance of JA was lower in 4110S under restrictive conditions (high temperature) than permissive conditions (low temperature). A possible regulated network of pathways associated with male sterility was suggested. These results provided insights into the molecular mechanism of fertility conversion in the thermosensitive male sterility system.

Keywords

Hybrid wheat Jasmonic acid Phenylpropanoid Thermosensitive male sterility 

Abbreviations

DEG

differentially expressed gene

GO

Gene Ontology

JA

jasmonic acid

TGMS

thermo-sensitive genic male sterility

EGMS

environmental-sensitive genic male sterility

PAL

phenylalanine ammonia-lyase

4CL

4-coumarate:coenzyme A ligase

LOX

lipoxygenase

AOS

allene oxide synthase

AOC

allene oxide cyclase

OPR

12-oxo-phytodienoic acid reductase

KOG

Eukaryotic Orthologous Groups

HCT

O-hydroxycinnamoyltransferase

AOS

allene oxide synthase

qRT-PCR

quantitative real-time PCR

DAPI

4′,6-diamidino-2-phenylindole

KCS

3-ketoacyl-CoA synthase

KAR

17-beta-estradiol 17-dehydrogenase

ELISA

enzyme-linked immunosorbent assay

FDR

false discovery rate

Notes

Acknowledgments

We thank Beijing BioMarker Company for their help with high-throughput sequencing. The data from this study was deposited in NCBI Sequence Read Archive under accession SRA: SRP211924. The line 4110S was presented by Dr. P.H. Dong from the College of Agronomy, Henan University of Science and Technology, China.

Funding information

This study was supported by the National Natural Science Foundation of China (31771874) and the Program in Science and Technology of Yangling State Demonstration Zone of Agricultural High-tech Industries (2018NY-19).

Compliance with ethical standards

All experiments were carried out with the approval of Northwest A&F University.

Competing interest

The authors declare that they have no competing interests.

Supplementary material

10142_2019_722_MOESM1_ESM.pdf (175 kb)
Supplementary Table S1 Sequence-specific primers used for qRT-PCR (PDF 117 kb)
10142_2019_722_MOESM2_ESM.pdf (158 kb)
Supplementary Table S2 Gene Ontology (GO) classifications of differentially expressed genes (PDF 174 kb)
10142_2019_722_MOESM3_ESM.pdf (117 kb)
Supplementary Table S3 Eukaryotic Orthologous Groups (KOG) functional classifications of annotated differentially expressed genes (PDF 158 kb)
10142_2019_722_MOESM4_ESM.pdf (146 kb)
Supplementary Table S4 Transcript facror IDs and corresponding families (PDF 198 kb)
10142_2019_722_MOESM5_ESM.pdf (116 kb)
Supplementary Table S5 KEGG pathways and DEGs number (PDF 133 kb)
10142_2019_722_MOESM6_ESM.pdf (199 kb)
Supplementary Table S6 Genes and KEGG terms in networks (PDF 116 kb)
10142_2019_722_MOESM7_ESM.pdf (579 kb)
Supplementary Fig. S1 The GO enrichment of biological processes (PDF 578 kb)
10142_2019_722_MOESM8_ESM.pdf (487 kb)
Supplementary Fig. S2 The GO enrichment of cellular components (PDF 486 kb)
10142_2019_722_MOESM9_ESM.pdf (356 kb)
Supplementary Fig. S3 The GO enrichment of molecular functions (PDF 356 kb)
10142_2019_722_MOESM10_ESM.pdf (136 kb)
Supplementary File S1 The detailed experimental methods. (PDF 135 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Xuetong Yang
    • 1
  • Jiali Ye
    • 1
  • Lingli Zhang
    • 1
  • Xiyue Song
    • 1
    Email author
  1. 1.College of AgronomyNorthwest A&F UniversityYanglingChina

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