Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis

Yan, He1; Zhuang, Menglong1; Xu, Xiaoyu1; Li, Shanshan1; Yang, Mingkang1,2; Li, Nianle1; Du, Xiaojuan1; Hu, Kangwei1; Peng, Xiaomin1; Huang, Wei1,2; Wu, Hong1,2; Tse, Yu Chung3; Zhao, Lifeng1; Wang, Hao1

2022-07-01

10.1080/15548627.2022.2095838

Autophagy   Impact Factor & Quartile

1554-8627

1554-8635

Macroautophagy/autophagy, a major catabolic pathway in eukaryotes, participates in plant sexual reproduction including the processes of male gametogenesis and the self-incompatibility response. Rapid pollen tube growth is another essential reproductive process that is metabolically highly demanding to drive the vigorous cell growth for delivery of male gametes for fertilization in angiosperms. Whether and how autophagy operates to maintain the homeostasis of pollen tubes remains unknown. Here, we provide evidence that autophagy is elevated in growing pollen tubes and critically required during pollen tube growth and male fertility in Arabidopsis. We demonstrate that SH3P2, a critical non-ATG regulator of plant autophagy, colocalizes with representative ATG proteins during autophagosome biogenesis in growing pollen tubes. Downregulation of SH3P2 expression significantly disrupts Arabidopsis pollen germination and pollen tube growth. Further analysis of organelle dynamics reveals crosstalk between autophagosomes and prevacuolar compartments following the inhibition of phosphatidylinositol 3-kinase. In addition, time-lapse imaging and tracking of ATG8e-labeled autophagosomes and depolarized mitochondria demonstrate that they interact specifically via the ATG8-family interacting motif (AIM)-docking site to mediate mitophagy. Ultrastructural identification of mitophagosomes and two additional forms of autophagosomes imply that multiple types of autophagy are likely to function simultaneously within pollen tubes. Altogether, our results suggest that autophagy is functionally crucial for mediating mitochondrial quality control and canonical cytoplasm recycling during pollen tube growth.

Arabidopsis ATG8e autophagy male fertility mitophagy pollen tube growth

SCI

English

Others

National Natural Science Foundation of China["91954110","31770196"] ; Natural Science Foundation of Guangdong Province[2021A1515012066]

Cell Biology

Cell Biology

WOS:000823401600001

TAYLOR & FRANCIS INC

Web of Science

1.South China Agr Univ, Coll Life Sci, Dept Cell & Dev Biol, Hong Kong, Peoples R China
2.South China Agr Univ, State Key Lab Conservat & Utilizat Subtrop Agrobi, Guangzhou, Peoples R China
3.Southern Univ Sci & Technol, Core Res Facil, Shenzhen, Guangdong, Peoples R China

Yan, He,Zhuang, Menglong,Xu, Xiaoyu,et al. Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis[J]. Autophagy,2022.

Yan, He.,Zhuang, Menglong.,Xu, Xiaoyu.,Li, Shanshan.,Yang, Mingkang.,...&Wang, Hao.(2022).Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis.Autophagy.

Yan, He,et al."Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis".Autophagy (2022).