Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation

Shuangshuang Wang, Jianan Lu, Xiu Fen Song, Shi Chao Ren, Chenjiang You, Jie Xu, Chun Ming Liu, Hong Ma, Fang Chang

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

The CLAVATA3/ESR-RELATED (CLE) peptide signals are required for cell-cell communication in several plant growth and developmental processes. However, little is known regarding the possible functions of the CLEs in the anther. Here, we show that a T-DNA insertional mutant, and dominant-negative (DN) and overexpression (OX) transgenic plants of the CLE19 gene, exhibited significantly reduced anther size and pollen grain number and abnormal pollen wall formation in Arabidopsis (Arabidopsis thaliana). Interestingly, the DN-CLE19 pollen grains showed a more extensively covered surface, but CLE19-OX pollen exine exhibited clearly missing connections in the network and lacked separation between areas that normally form the lacunae. With a combination of cell biological, genetic, and transcriptomic analyses on cle19, DN-CLE19, and CLE19-OX plants, we demonstrated that CLE19-OX plants produced highly vacuolated and swollen aborted microspores (ams)-like tapetal cells, lacked lipidic tapetosomes and elaioplasts, and had abnormal pollen primexine without obvious accumulation of sporopollenin precursors. Moreover, CLE19 is important for the normal expression of more than 1,000 genes, including the transcription factor gene AMS, 280 AMS-downstream genes, and other genes involved in pollen coat and pollen exine formation, lipid metabolism, pollen germination, and hormone metabolism. In addition, the DN-CLE19(+/+) ams(-/-) plants exhibited the ams anther phenotype and ams(+/-) partially suppressed the DN-CLE19 transgeneinduced pollen exine defects. These findings demonstrate that the proper amount of CLE19 signal is essential for the normal expression of AMS and its downstream gene networks in the regulation of anther development and pollen exine formation.

Original languageEnglish (US)
Pages (from-to)1186-1202
Number of pages17
JournalPlant physiology
Volume175
Issue number3
DOIs
StatePublished - Nov 1 2017

Fingerprint

exine
Pollen
transcriptomics
pollen
microspores
anthers
genes
elaioplasts
Arabidopsis
Genes
hormone metabolism
cell communication
pollen germination
Plant Genes
signal peptide
lipid metabolism
Gene Regulatory Networks
Genetically Modified Plants
transgenic plants
Germination

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Wang, S., Lu, J., Song, X. F., Ren, S. C., You, C., Xu, J., ... Chang, F. (2017). Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation. Plant physiology, 175(3), 1186-1202. https://doi.org/10.1104/pp.17.00439
Wang, Shuangshuang ; Lu, Jianan ; Song, Xiu Fen ; Ren, Shi Chao ; You, Chenjiang ; Xu, Jie ; Liu, Chun Ming ; Ma, Hong ; Chang, Fang. / Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation. In: Plant physiology. 2017 ; Vol. 175, No. 3. pp. 1186-1202.
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abstract = "The CLAVATA3/ESR-RELATED (CLE) peptide signals are required for cell-cell communication in several plant growth and developmental processes. However, little is known regarding the possible functions of the CLEs in the anther. Here, we show that a T-DNA insertional mutant, and dominant-negative (DN) and overexpression (OX) transgenic plants of the CLE19 gene, exhibited significantly reduced anther size and pollen grain number and abnormal pollen wall formation in Arabidopsis (Arabidopsis thaliana). Interestingly, the DN-CLE19 pollen grains showed a more extensively covered surface, but CLE19-OX pollen exine exhibited clearly missing connections in the network and lacked separation between areas that normally form the lacunae. With a combination of cell biological, genetic, and transcriptomic analyses on cle19, DN-CLE19, and CLE19-OX plants, we demonstrated that CLE19-OX plants produced highly vacuolated and swollen aborted microspores (ams)-like tapetal cells, lacked lipidic tapetosomes and elaioplasts, and had abnormal pollen primexine without obvious accumulation of sporopollenin precursors. Moreover, CLE19 is important for the normal expression of more than 1,000 genes, including the transcription factor gene AMS, 280 AMS-downstream genes, and other genes involved in pollen coat and pollen exine formation, lipid metabolism, pollen germination, and hormone metabolism. In addition, the DN-CLE19(+/+) ams(-/-) plants exhibited the ams anther phenotype and ams(+/-) partially suppressed the DN-CLE19 transgeneinduced pollen exine defects. These findings demonstrate that the proper amount of CLE19 signal is essential for the normal expression of AMS and its downstream gene networks in the regulation of anther development and pollen exine formation.",
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Wang, S, Lu, J, Song, XF, Ren, SC, You, C, Xu, J, Liu, CM, Ma, H & Chang, F 2017, 'Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation', Plant physiology, vol. 175, no. 3, pp. 1186-1202. https://doi.org/10.1104/pp.17.00439

Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation. / Wang, Shuangshuang; Lu, Jianan; Song, Xiu Fen; Ren, Shi Chao; You, Chenjiang; Xu, Jie; Liu, Chun Ming; Ma, Hong; Chang, Fang.

In: Plant physiology, Vol. 175, No. 3, 01.11.2017, p. 1186-1202.

Research output: Contribution to journalArticle

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AU - Wang, Shuangshuang

AU - Lu, Jianan

AU - Song, Xiu Fen

AU - Ren, Shi Chao

AU - You, Chenjiang

AU - Xu, Jie

AU - Liu, Chun Ming

AU - Ma, Hong

AU - Chang, Fang

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AB - The CLAVATA3/ESR-RELATED (CLE) peptide signals are required for cell-cell communication in several plant growth and developmental processes. However, little is known regarding the possible functions of the CLEs in the anther. Here, we show that a T-DNA insertional mutant, and dominant-negative (DN) and overexpression (OX) transgenic plants of the CLE19 gene, exhibited significantly reduced anther size and pollen grain number and abnormal pollen wall formation in Arabidopsis (Arabidopsis thaliana). Interestingly, the DN-CLE19 pollen grains showed a more extensively covered surface, but CLE19-OX pollen exine exhibited clearly missing connections in the network and lacked separation between areas that normally form the lacunae. With a combination of cell biological, genetic, and transcriptomic analyses on cle19, DN-CLE19, and CLE19-OX plants, we demonstrated that CLE19-OX plants produced highly vacuolated and swollen aborted microspores (ams)-like tapetal cells, lacked lipidic tapetosomes and elaioplasts, and had abnormal pollen primexine without obvious accumulation of sporopollenin precursors. Moreover, CLE19 is important for the normal expression of more than 1,000 genes, including the transcription factor gene AMS, 280 AMS-downstream genes, and other genes involved in pollen coat and pollen exine formation, lipid metabolism, pollen germination, and hormone metabolism. In addition, the DN-CLE19(+/+) ams(-/-) plants exhibited the ams anther phenotype and ams(+/-) partially suppressed the DN-CLE19 transgeneinduced pollen exine defects. These findings demonstrate that the proper amount of CLE19 signal is essential for the normal expression of AMS and its downstream gene networks in the regulation of anther development and pollen exine formation.

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