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Tip growth defective1 interacts with cellulose synthase A3 to regulate cellulose biosynthesis in Arabidopsis

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AtTIP1 physically and genetically interacts with AtCESA3. AtCESA3 undergoes S-acylation, possibly mediated by AtTIP1, suggesting a specific role of AtTIP1 in cellulose biosynthesis and plant development.

Abstract

S-acylation is a reversible post-translational lipid modification of proteins catalyzed by protein S-acyl transferases (PATs). S-acylation is important for various biological molecular mechanisms including cellulose biosynthesis. Cellulose is synthesized by the cellulose synthase A (CESA) complexes (CSCs) at the plasma membrane. However, specific PAT involving in cellulose biosynthesis has not been identified and the precise mechanism by which PAT regulates the CESAs is largely unknown. Here, we report isolation of tip1-5, an allele of Tip Growth Defective1 (AtTIP1/AtPAT24) with a premature stop codon. tip1-5 genetically interacts with ixr1-2, a point mutant of AtCESA3 which encodes a catalytic subunit of CSC synthesizing primary wall cellulose. We show that AtTIP1 physically interacts with AtCESA3. AtCESA3 undergoes S-acylation, which is possibly mediated by AtTIP1, suggesting a functional relationship between AtTIP1 and AtCESA3. Moreover, the interfascicular fiber cells in the primary inflorescence stems of tip1-5 ixr1-2 double mutant contain thinner cell walls and significantly less crystalline cellulose compared to the single mutants. These results highlight the positive regulation of AtTIP1 in cellulose biosynthesis, and a specific role of AtPAT in plant development.

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Acknowledgements

We thank Dr. Yunde Zhao and Dr. Yongbiao Xue for insightful discussion, Drs. Sha Li and Shanwei Li for tip1-4 seeds, Dr. Feng Qin for tip1-3 seeds, Dr. Jianmin Zhou for LCI vector, Dr. Yuxin Hu for the Chemiluminescent Imaging System, Dr. Caiji Gao for suggestions and EMP12 plasmid. We thank Ms. Fengqin Dong from the Plant Science Facility of the Institute of Botany, Chinese Academy of Sciences, and Ms. Lizhen Song for their excellent technical assistance. This work was supported by the projects from the National Natural Science Foundation of China (NSFC) (31970309; 31171389), National Key Research and Development Program of China (2016YFD0100400), Strategic Priority Research Program of the Chinese Academy of Sciences (XDA26030302), and STS Program of the Chinese Academy of Sciences (STS Program KFJ-STS-ZDTP-076 to Y.C.). Madhu Shudan Thapa Magar was supported by the PhD fellowship of CAS-TWAS President’s Fellowship program.

Funding

National Natural Science Foundation of China (Grant Nos. 31970309, 31171389). National Key Research and Development Program of China (2016YFD0100400), Strategic Priority Research Program of the Chinese Academy of Sciences (XDA26030302), and STS Program of the Chinese Academy of Sciences (STS Program KFJ-STS-ZDTP-076 to Y.C.).

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Authors and Affiliations

  1. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Lu Zhang, Madhu Shudan Thapa Magar, Yanning Wang & Youfa Cheng

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Lu Zhang, Madhu Shudan Thapa Magar, Yanning Wang & Youfa Cheng

  3. Department of Plant Resources, Ministry of Forests and Environment, Government of Nepal, Kathmandu, 44600, Nepal

    Madhu Shudan Thapa Magar

  4. Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China

    Youfa Cheng

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  1. Lu Zhang
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Contributions

YC designed the research. LZ, MSTM and YW performed experiments. YC, LZ and MSTM analyzed data, and YC, LZ and MSTM wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Youfa Cheng.

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Accession numbers

Sequence data of the genes described in this article can be found in the GenBank/EMBL data libraries under the accession numbers: AT5G20350 (AtTIP1), AT5G05170 (AtCESA3), AT4G32410 (AtCESA1), and AT5G64740 (AtCESA6).

Lu Zhang and Madhu Shudan Thapa Magar contributed equally as co-first authors to this work.

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Zhang, L., Thapa Magar, M.S., Wang, Y. et al. Tip growth defective1 interacts with cellulose synthase A3 to regulate cellulose biosynthesis in Arabidopsis. Plant Mol Biol 110, 1–12 (2022). https://doi.org/10.1007/s11103-022-01283-8

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