The Pumilio RNA-binding protein APUM24 regulates seed maturation by fine-tuning the BPM-WRI1 module in Arabidopsis

Ruihua Huang, Mengling Liu, Guanping Gong, Pingzhi Wu, Barunava Patra, Ling Yuan, Hongting Qin, Xiaoxu Wang, Guohe Wang, Huimei Liao, Lu Gao, Chengwei Yang, Hongqing Li, Shengchun Zhang

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Pumilio RNA-binding proteins participate in messenger RNA (mRNA) degradation and translational repression, but their roles in plant development are largely unclear. Here, we show that Arabidopsis PUMILIO PROTEIN24 (APUM24), an atypical Pumilio-homology domain-containing protein, plays an important part in regulating seed maturation, a major stage of plant development. APUM24 is strongly expressed in maturing seeds. Reducing APUM24 expression resulted in abnormal seed maturation, wrinkled seeds, and lower seed oil contents, and APUM24 knockdown resulted in lower levels of WRINKLED 1 (WRI1), a key transcription factor controlling seed oil accumulation, and lower expression of WRI1 target genes. APUM24 reduces the mRNA stability of BTB/POZMATH (BPM) family genes, thus decreasing BPM protein levels. BPM is responsible for the 26S proteasome-mediated degradation of WRI1 and has important functions in plant growth and development. The 3′ untranslated regions of BPM family genes contain putative Pumilio response elements (PREs), which are bound by APUM24. Reduced BPM or increased WRI1 expression rescued the deficient seed maturation of apum24-2 knockdown mutants, and APUM24 overexpression resulted in increased seed size and weight. Therefore, APUM24 is crucial to seed maturation through its action as a positive regulator fine-tuning the BPM-WRI1 module, making APUM24 a promising target for breeding strategies to increase crop yields.

Original languageEnglish
Pages (from-to)1240-1259
Number of pages20
JournalJournal of Integrative Plant Biology
Volume63
Issue number7
DOIs
StatePublished - Jul 2021

Bibliographical note

Funding Information:
We thank Professor Hanjo A. Hellmann from the Washington State University for providing the artificial microRNA vector, Professor Andrzej Wierzbicki from the University of Michigan for technical support for the RIP experiment, and the ABRC for kindly providing seeds used in this study. This work is supported by the National Natural Science Foundation of China (31870301, 31370350 for S.Z., and 31871222 for C.Y.), the Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2016 for S.Z.), and the award from the Program for Changjiang Scholars (2017 for C.Y.).

Funding Information:
We thank Professor Hanjo A. Hellmann from the Washington State University for providing the artificial microRNA vector, Professor Andrzej Wierzbicki from the University of Michigan for technical support for the RIP experiment, and the ABRC for kindly providing seeds used in this study. This work is supported by the National Natural Science Foundation of China (31870301, 31370350 for S.Z., and 31871222 for C.Y.), the Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2016 for S.Z.), and the award from the Program for Changjiang Scholars (2017 for C.Y.).

Publisher Copyright:
© 2021 Institute of Botany, Chinese Academy of Sciences

Keywords

  • APUM24
  • Arabidopsis
  • BPM
  • RNA-binding protein
  • WRI1
  • seed maturation

ASJC Scopus subject areas

  • Biochemistry
  • Biochemistry, Genetics and Molecular Biology (all)
  • Plant Science

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