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Transcriptome profiling of developmental leaf senescence in sorghum (Sorghum bicolor)

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Leaf senescence is essential for the nutrient economy of crops and is executed by so-called senescence-associated genes (SAGs). Here we explored the monocot C4 model crop Sorghum bicolor for a holistic picture of SAG profiles by RNA-seq. Leaf samples were collected at four stages during developmental senescence, and in total, 3396 SAGs were identified, predominantly enriched in GO categories of metabolic processes and catalytic activities. These genes were enriched in 13 KEGG pathways, wherein flavonoid and phenylpropanoid biosynthesis and phenylalanine metabolism were overrepresented. Seven regions on Chromosomes 1, 4, 5 and 7 contained SAG ‘hotspots’ of duplicated genes or members of cupin superfamily involved in manganese ion binding and nutrient reservoir activity. Forty-eight expression clusters were identified, and the candidate orthologues of the known important senescence transcription factors such as ORE1, EIN3 and WRKY53 showed “SAG” expression patterns, implicating their possible roles in regulating sorghum leaf senescence. Comparison of developmental senescence with salt- and dark- induced senescence allowed for the identification of 507 common SAGs, 1996 developmental specific SAGs as well as 176 potential markers for monitoring senescence in sorghum. Taken together, these data provide valuable resources for comparative genomics analyses of leaf senescence and potential targets for the manipulation of genetic improvement of Sorghum bicolor.

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Abbreviations

cDNA:

Complementary DNA

DEGs:

Differentially expressed genes

DGE:

Digital gene expression

ES:

Early senescence

FDR:

False discovery rate

FPKM:

Fragment per kilo base per million mapped fragment

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

LS:

Late senescence

MS:

Middle senescence

NGS:

Next-generation sequencing

QTL:

Quantitative trait locus

SAGs:

Senescence-associated genes

TF:

Transcription factor

TFBS:

Transcription factor binding site

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Acknowledgments

Members of Hai-Chun Jing’s lab are acknowledged for stimulating discussion on this project. This work was partially funded by grants to Hai-Chun Jing from National Natural Science Foundation of China (31271797, 30970252 and 31471570) and Ministry of Science and Technology of the People’s Republic of China (2013BAD22B01, 2015BAD15B03). We are also grateful to the handling editor and two anonymous reviewers for their critical comments and useful suggestions on a previous version of the manuscript.

Author contributions

Hai-Chun Jing designed and conceived the research, Wei-Juan Hu and Li-dong Wang performed the experiments, Xiao-yuan Wu and Hong Luo analysed the sequencing data, Yan Xia, Yi Zhao, Li-min Zhang, Jing-Chu Luo and Hai-Chun Jing assisted data analysing and gave thoughtful discussion. Xiao-Yuan Wu, Hong Luo and Hai-Chun Jing wrote the whole paper with feedback from Jing-Chu Luo. Xiao-Yuan Wu, Wei-Juan Hu, and Hong Luo contributed equally to the paper.

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Author notes

  1. Wei-Juan Hu

    Present address: Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, People’s Republic of China

Authors and Affiliations

  1. Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

    Xiao-Yuan Wu, Wei-Juan Hu, Hong Luo, Yan Xia, Li-Dong Wang, Li-Min Zhang & Hai-Chun Jing

  2. College of Life Sciences and State Key Laboratory of Protein and Plant Gene Research, Peking University, Beijing, 100871, People’s Republic of China

    Yi Zhao & Jing-Chu Luo

  3. Inner Mongolia Research Centre for Practaculture, Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

    Xiao-Yuan Wu, Hong Luo, Yan Xia, Li-Dong Wang, Li-Min Zhang & Hai-Chun Jing

  4. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Xiao-Yuan Wu

Authors
  1. Xiao-Yuan Wu
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  2. Wei-Juan Hu
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  3. Hong Luo
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  4. Yan Xia
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  5. Yi Zhao
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  6. Li-Dong Wang
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  7. Li-Min Zhang
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  8. Jing-Chu Luo
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  9. Hai-Chun Jing
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Corresponding authors

Correspondence to Jing-Chu Luo or Hai-Chun Jing.

Additional information

Xiao-Yuan Wu, Wei-Juan Hu and Hong Luo have contributed equally to this work.

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11103_2016_532_MOESM6_ESM.eps

ESM Fig. S1 Conditions shared and specific SAGs. A Venn diagram showing the numbers of SAGs shared by and specific to developmental, dark- and salt-induced senescence, respectively. DSAGs represents developmental specific SAGs (EPS 21034 KB)

ESM Fig. S2 Number of expressed genes of different expression value regions in each stage (EPS 3040 KB)

11103_2016_532_MOESM8_ESM.eps

ESM Fig. S3 Number of SAGs contain three kinds of binding motifs. Candidate targets of transcription factors were identified by searching transcription factors binding sites in 2 kb promoter region of each sorghum gene (EPS 20871 KB)

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Wu, XY., Hu, WJ., Luo, H. et al. Transcriptome profiling of developmental leaf senescence in sorghum (Sorghum bicolor). Plant Mol Biol 92, 555–580 (2016). https://doi.org/10.1007/s11103-016-0532-1

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  • DOI: https://doi.org/10.1007/s11103-016-0532-1

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