Sperm-origin paternal effects on root stem cell niche differentiation

Tianhe Cheng, Zhenzhen Liu, Haiming Li, Xiaorong Huang, Wei Wang, Ce Shi, Xuecheng Zhang, Hong Chen, Zhuang Yao, Peng Zhao, Xiongbo Peng and Meng-Xiang Sun ()
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Tianhe Cheng: Wuhan University
Zhenzhen Liu: Wuhan University
Haiming Li: Wuhan University
Xiaorong Huang: Wuhan University
Wei Wang: Wuhan University
Ce Shi: Wuhan University
Xuecheng Zhang: Wuhan University
Hong Chen: Wuhan University
Zhuang Yao: Wuhan University
Peng Zhao: Wuhan University
Xiongbo Peng: Wuhan University
Meng-Xiang Sun: Wuhan University

Nature, 2024, vol. 634, issue 8032, 220-227

Abstract: Abstract Fertilization introduces parental genetic information into the zygote to guide embryogenesis. Parental contributions to postfertilization development have been discussed for decades, and the data available show that both parents contribute to the zygotic transcriptome, suggesting a paternal role in early embryogenesis1–6. However, because the specific paternal effects on postfertilization development and the molecular pathways underpinning these effects remain poorly understood, paternal contribution to early embryogenesis and plant development has not yet been adequately demonstrated7. Here our research shows that TREE1 and its homologue DAZ3 are expressed exclusively in Arabidopsis sperm. Despite presenting no evident defects in sperm development and fertilization, tree1 daz3 unexpectedly led to aberrant differentiation of the embryo root stem cell niche. This defect persisted in seedlings and disrupted root tip regeneration, comparable to congenital defects in animals. TREE1 and DAZ3 function by suppression of maternal RKD2 transcription, thus mitigating the detrimental maternal effects from RKD2 on root stem cell niche. Therefore, our findings illuminate how genetic deficiencies in sperm can exert enduring paternal effects on specific plant organ differentiation and how parental-of-origin genes interact to ensure normal embryogenesis. This work also provides a new concept of how gamete quality or genetic deficiency can affect specific plant organ formation.

Date: 2024
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DOI: 10.1038/s41586-024-07885-0

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