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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

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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.

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Abbreviations

CMS:

Cytoplasmic male sterility

PPR:

Pentatricopeptide repeat

DPA:

Days post-anthesis

BILs:

Backcross inbred lines

Rf:

Restorer of fertility

DEG:

Differentially expressed gene

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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).

Author information

Authors and Affiliations

  1. Department of Plant and Environmental Sciences, New Mexico State University, Las Cruces, 88003, USA

    Zongfu Han & Jinfa Zhang

  2. Cotton Research Center, Shandong Academy of Agricultural Sciences, Jinan, 250100, China

    Zongfu Han & Ruzhong Li

  3. School of Biological Science and Technology, University of Jinan, Jinan, 250022, China

    Yuxiang Qin

  4. State Key Laboratory of Cotton Biology, Institute of Cotton Research (ICR), Chinese Academy of Agricultural Sciences (CAAS), Anyang, 455000, China

    Xihua Li, Jiwen Yu, Chaozhu Xing & Jianyong Wu

  5. Department of Computer Science, New Mexico State University, Las Cruces, 88003, USA

    Mingzhou Song

Authors
  1. Zongfu Han
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  2. Yuxiang Qin
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  3. Xihua Li
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  4. Jiwen Yu
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  7. Mingzhou Song
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  9. Jinfa Zhang
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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.

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Correspondence to Zongfu Han or Jinfa Zhang.

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Han, Z., Qin, Y., Li, X. et al. 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. Mol Genet Genomics 295, 55–66 (2020). https://doi.org/10.1007/s00438-019-01604-5

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