Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

Di Wu; Yiming Wei; Xiangyu Zhao; Boka Li; Huankai Zhang; Gang Xu; Juntong Lv; Dajian Zhang; Xiansheng Zhang; Min Ni

doi:10.1016/j.molp.2022.09.002

Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

Di Wu, Yiming Wei, Xiangyu Zhao, Boka Li, Huankai Zhang, Gang Xu, Juntong Lv, Dajian Zhang, Xiansheng Zhang, Min Ni

Plant and Microbial Biology

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies.

Original language	English (US)
Pages (from-to)	1575-1589
Number of pages	15
Journal	Molecular Plant
Volume	15
Issue number	10
DOIs	https://doi.org/10.1016/j.molp.2022.09.002
State	Published - Oct 3 2022

Bibliographical note

Funding Information:
We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.).

Funding Information:
We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.).

Publisher Copyright:
© 2022 The Author

Keywords

Brassicales
Fabales
IKU2
MEDEA
Poales
endosperm

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10.1016/j.molp.2022.09.002

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title = "Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution",

abstract = "Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies.",

keywords = "Brassicales, Fabales, IKU2, MEDEA, Poales, endosperm",

author = "Di Wu and Yiming Wei and Xiangyu Zhao and Boka Li and Huankai Zhang and Gang Xu and Juntong Lv and Dajian Zhang and Xiansheng Zhang and Min Ni",

note = "Funding Information: We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.). Funding Information: We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.). Publisher Copyright: {\textcopyright} 2022 The Author",

year = "2022",

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doi = "10.1016/j.molp.2022.09.002",

language = "English (US)",

volume = "15",

pages = "1575--1589",

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number = "10",

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T1 - Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

AU - Wu, Di

AU - Wei, Yiming

AU - Zhao, Xiangyu

AU - Li, Boka

AU - Zhang, Huankai

AU - Xu, Gang

AU - Lv, Juntong

AU - Zhang, Dajian

AU - Zhang, Xiansheng

AU - Ni, Min

N1 - Funding Information: We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.). Funding Information: We thank Professor Ramin Yadegari at the University of Arizona for Atmedea-3 seeds. We thank Professor Hongzhi Kong at the University of the Chinese Academy of Sciences for IKU2 and MEDEA phylogenetic tree analysis. This work was supported by grants from the National Natural Science Foundation of China 32071921 (X.Y.Z.), National Key Research and Development Program 2021YFF1001203 (D.J.Z.), National Natural Science Foundation of China 31730008 (X.S.Z.), and National Science Foundation IOS-1933291 (M.N.). Publisher Copyright: © 2022 The Author

PY - 2022/10/3

Y1 - 2022/10/3

N2 - Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies.

AB - Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies.

KW - Brassicales

KW - Fabales

KW - IKU2

KW - MEDEA

KW - Poales

KW - endosperm

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DO - 10.1016/j.molp.2022.09.002

M3 - Article

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AN - SCOPUS:85139119449

SN - 1674-2052

VL - 15

SP - 1575

EP - 1589

JO - Molecular Plant

JF - Molecular Plant

IS - 10

ER -

Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

Abstract

Bibliographical note

Keywords

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