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

doi:10.1111/jipb.13092

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 journal › Article › peer-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 language	English
Pages (from-to)	1240-1259
Number of pages	20
Journal	Journal of Integrative Plant Biology
Volume	63
Issue number	7
DOIs	https://doi.org/10.1111/jipb.13092
State	Published - 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

Access to Document

10.1111/jipb.13092

Cite this

@article{529cf5f4742e4e12b0aadb9a8625455a,

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

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.",

keywords = "APUM24, Arabidopsis, BPM, RNA-binding protein, WRI1, seed maturation",

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

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: {\textcopyright} 2021 Institute of Botany, Chinese Academy of Sciences",

year = "2021",

month = jul,

doi = "10.1111/jipb.13092",

language = "English",

volume = "63",

pages = "1240--1259",

number = "7",

}

TY - JOUR

T1 - The Pumilio RNA-binding protein APUM24 regulates seed maturation by fine-tuning the BPM-WRI1 module in Arabidopsis

AU - Huang, Ruihua

AU - Liu, Mengling

AU - Gong, Guanping

AU - Wu, Pingzhi

AU - Patra, Barunava

AU - Yuan, Ling

AU - Qin, Hongting

AU - Wang, Xiaoxu

AU - Wang, Guohe

AU - Liao, Huimei

AU - Gao, Lu

AU - Yang, Chengwei

AU - Li, Hongqing

AU - Zhang, Shengchun

N1 - 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

PY - 2021/7

Y1 - 2021/7

N2 - 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.

AB - 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.

KW - APUM24

KW - Arabidopsis

KW - BPM

KW - RNA-binding protein

KW - WRI1

KW - seed maturation

UR - http://www.scopus.com/inward/record.url?scp=85107139892&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85107139892&partnerID=8YFLogxK

U2 - 10.1111/jipb.13092

DO - 10.1111/jipb.13092

M3 - Article

C2 - 33729679

AN - SCOPUS:85107139892

VL - 63

SP - 1240

EP - 1259

IS - 7

ER -

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this