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A genome-wide analysis of pentatricopeptide repeat (PPR) protein-encoding genes in four Gossypium species with an emphasis on their expression in floral buds, ovules, and fibers in upland cotton

  • Zongfu HanEmail author
  • Yuxiang Qin
  • Xihua Li
  • Jiwen Yu
  • Ruzhong Li
  • Chaozhu Xing
  • Mingzhou Song
  • Jianyong Wu
  • Jinfa ZhangEmail author
Original Article
  • 245 Downloads

Abstract

Cotton is the most important natural fiber used in textiles. Breeding for “three-lines”, i.e., cytoplasmic male sterility (CMS)-based sterile (A), maintainer (B), and restorer (R) line, is a promising approach to harness hybrid vigor in cotton. Pentatricopeptide repeat (PPR) protein-encoding genes play an important role in plant growth and development including restoration of CMS plants to male fertility. However, PPRs, especially those contributing to CMS and fiber development, remain largely unknown in cotton. In this study, a genome-wide identification and characterization of PPR gene family in four Gossypium species with genome sequences (G. arboreum, G. raimondii, G. hirsutum, and G. barbadense) were performed, and expressed PPR genes in developing floral buds, ovules, and fibers were compared to identify possible PPRs related to CMS restoration and fiber development. A total of 539, 558, 1032, and 1055 PPRs were predicted in the above four species, respectively, which were further mapped to chromosomes for a synteny analysis. Through an RNA-seq analysis, 86% (882) PPRs were expressed in flowering buds of upland cotton (G. hirsutum); however, only 11 and 6 were differentially expressed (DE) between restorer R and its near-isogenic (NI) B and between R and its NI A line, respectively. Another RNA-seq analysis identified the expression of only 54% (556) PPRs in 0 and 3 day(s) post-anthesis (DPA) ovules and 24% (247) PPRs in 10 DPA fibers; however, only 59, 6, and 27 PPRs were DE in 0 and 3 DPA ovules, and 10 DPA fibers between two backcross inbred lines (BILs) with differing fiber length, respectively. Only 2 PPRs were DE between Xuzhou 142 and its fiberless and fuzzless mutant. Quantitative RT-PCR analysis confirmed the validity of the RNA-seq results for the gene expression pattern. Therefore, only a very small number of PPRs may be associated with fertility restoration of CMS and genetic differences in fiber initiation and elongation. These results lay a foundation for understanding the roles of PPR genes in cotton, and will be useful in the prioritization of candidate PPR gene functional validation for cotton CMS restoration and fiber development.

Keywords

Gossypium Pentatricopeptide repeat (PPR) protein gene family Phylogenetic analysis Cytoplasmic male sterility (CMS) Fiber development 

Abbreviations

CMS

Cytoplasmic male sterility

PPR

Pentatricopeptide repeat

DPA

Days post-anthesis

BILs

Backcross inbred lines

Rf

Restorer of fertility

DEG

Differentially expressed gene

Notes

Authors′ contributions

Zongfu Han performed the study, analyzed pentatricopeptide repeat (PPR) protein-encoding genes in Gossypium species, and drafted the manuscript. Yuxiang Qin helped in synteny analysis of PPR genes and edited the manuscript. Xihua Li collected (ovules and fibers) samples and extracted RNA, and analyzed RNA-Seq data. Jiwen Yu collected flowering buds, extracted RNA and analyzed RNA-Seq data. Ruzhong Li assisted Xinhua Li in collecting samples; Chaozhu Xing assisted Jiwen Yu in sample collection and RNA extraction. Mingzhou Song assisted Li and Yu in finding of DEGs from the RNA-seq raw data, Jianyong Wu helped to add detailed information on RNA-seq experiment. Jinfa Zhang conceived the project and revised the manuscript. All authors read and approved the manuscript.

Funding

This work was financially supported by National Natural Science Foundation of China (31240011), the Youth Scientific Research Foundation of Shandong Academy of Agricultural Sciences (2014QNM05), and Natural Science Foundation of Shandong Province (BS2011NY09).

Compliance with ethical standards

Informed consent

Not applicable.

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

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Copyright information

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

Authors and Affiliations

  1. 1.Department of Plant and Environmental SciencesNew Mexico State UniversityLas CrucesUSA
  2. 2.Cotton Research CenterShandong Academy of Agricultural SciencesJinanChina
  3. 3.School of Biological Science and TechnologyUniversity of JinanJinanChina
  4. 4.State Key Laboratory of Cotton BiologyInstitute of Cotton Research (ICR), Chinese Academy of Agricultural Sciences (CAAS)AnyangChina
  5. 5.Department of Computer ScienceNew Mexico State UniversityLas CrucesUSA

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