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Acyl-CoA synthetases from Physcomitrella, rice and Arabidopsis: different substrate preferences but common regulation by MS188 in sporopollenin synthesis

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Abstract

Main conclusion

ACOS5, OsACOS12 and PpACOS6 are all capable of fatty acyl-CoA synthetase activity but exhibit different substrate preferences. The transcriptional regulation of ACOS for sporopollenin synthesis appears to have been conserved in Physcomitrella, rice and Arabidopsis during evolution.

Abstract

Sporopollenin is the major constituent of spore and pollen exines. In Arabidopsis, acyl-CoA synthetase 5 (ACOS5) is an essential enzyme for sporopollenin synthesis, and its orthologues are PpACOS6 from the moss Physcomitrella and OsACOS12 from monocot rice. However, knowledge regarding the evolutionary conservation and divergence of the ACOS gene in sporopollenin synthesis remains limited. In this study, we analysed the function and regulation of PpACOS6 and OsACOS12. A complementation test showed that OsACOS12 driven by the ACOS5 promoter could partially restore the male fertility of the acos5 mutant in Arabidopsis, while PpACOS6 did not rescue the acos5 phenotype. ACOS5, PpACOS6 and OsACOS12 all complemented the acyl-CoA synthetase-deficient yeast strain (YB525) phenotype, although they exhibited different substrate preferences. To understand the conservation of sporopollenin synthesis regulation, we constructed two constructs with ACOS5 driven by the OsACOS12 or PpACOS6 promoter. Both constructs could restore the fertility of acos5 plants. The MYB transcription factor MS188 from Arabidopsis directly regulates ACOS5. We found that MS188 could also bind the promoters of OsACOS12 and PpACOS6 and activate the genes driven by the promoters, suggesting that the transcriptional regulation of these genes was similar to that of ACOS5. These results show that the ACOS gene promoter region from Physcomitrella, rice and Arabidopsis has been functionally conserved during evolution, while the chain lengths of fatty acid-derived monomers of sporopollenin vary in different plant species.

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Abbreviations

ACOS:

Acyl-CoA synthetase

AMS:

ABORTED MICROSPORES

LUC:

Firefly luciferase

MBP:

Maltose binding protein

MS:

MALE STERILE

SEM:

Scanning electron microscopy

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Funding

This study was financially supported by Zhejiang Provincial Nature Science (LQ19C030001), the National Science Foundation of China (31770348), ‘Chen Guang’ project (15CG50) and Innovation Program (2017-01-07-00-02-E00039) supported by Shanghai Municipal Education Commission and Shanghai Education Development Foundation. A grant from the Science and Technology Commission of Shanghai Municipality (18DZ2260500).

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  1. Yue-Ling Li and Yan-Fei Zhang have contributed equally to this work.

Authors and Affiliations

  1. Zhejiang Provincial Key Laboratory of Plant Evolutionary and Conservation, Taizhou University, Taizhou, 318000, China

    Yue-Ling Li

  2. Institute of Ecology, Taizhou University, Taizhou, 318000, China

    Yue-Ling Li

  3. Shanghai Key Laboratory of Plant Molecule Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, 200234, China

    Yan-Fei Zhang, Dan-Dan Li, Qiang-Sheng Shi, Yue Lou, Zhong-Nan Yang & Jun Zhu

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  1. Yue-Ling Li
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Correspondence to Jun Zhu.

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Fig. S1

Gene structure of ACOS5 and T-DNA insertion. The exons are shown as black boxes. The introns, promoter, and untranslated regions are shown as lines. T-DNA was inserted in the first exon. LP, left border primer; RP, right border primer (JPEG 782 kb)

Fig. S2

Analysis of the acos5−/− background in transgenic lines. PCR analysis of the acos5−/− background in the aproACOS5:OsACOS12, bproACOS5:PpACOS6, cproOsACOS12:ACOS5 and dproPpACOS6:ACOS5 transgenic lines. The lanes marked with yellow line indicate the homozygous acos5-/- background using LP/RP and LB/RP primers. The lanes marked with red line indicate acos5+/- heterozygous background using LP/RP and LB/RP primers (JPEG 3106 kb)

Fig. S3

Expression of ACOS5 in wild type and transgenic line. qRT-PCR analysis of ACOS5 expression in wild type and proOsACOS12:ACOS5 transgenic lines. The error bars indicate the standard deviations from three independent assays (JPEG 470 kb)

Fig. S4

Expression and purification of MS188 recombinant protein. The MS188 proteins from Arabidopsis and rice tagged with MBP, respectively, were inducted and purified in E. coli (JPEG 2814 kb)

Fig. S5

Diagram of the sequence alignment of the MS188 (Arabidopsis), OsMS188 (rice) and PpMS188 (Physcomitrella) proteins (JPEG 3292 kb)

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Li, YL., Zhang, YF., Li, DD. et al. Acyl-CoA synthetases from Physcomitrella, rice and Arabidopsis: different substrate preferences but common regulation by MS188 in sporopollenin synthesis. Planta 250, 535–548 (2019). https://doi.org/10.1007/s00425-019-03189-0

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