Sporophytic control of tapetal development and pollen fertility by a mitogen-activated protein kinase cascade in rice

J Integr Plant Biol. 2024 Jul;66(7):1500-1516. doi: 10.1111/jipb.13673. Epub 2024 May 15.

Abstract

Tapetum, the innermost layer of the anther wall, provides essential nutrients and materials for pollen development. Timely degradation of anther tapetal cells is a prerequisite for normal pollen development in flowering plants. Tapetal cells facilitate male gametogenesis by providing cellular contents after highly coordinated programmed cell death (PCD). Tapetal development is regulated by a transcriptional network. However, the signaling pathway(s) involved in this process are poorly understood. In this study, we report that a mitogen-activated protein kinase (MAPK) cascade composed of OsYDA1/OsYDA2-OsMKK4-OsMPK6 plays an important role in tapetal development and male gametophyte fertility. Loss of function of this MAPK cascade leads to anther indehiscence, enlarged tapetum, and aborted pollen grains. Tapetal cells in osmkk4 and osmpk6 mutants exhibit an increased presence of lipid body-like structures within the cytoplasm, which is accompanied by a delayed occurrence of PCD. Expression of a constitutively active version of OsMPK6 (CA-OsMPK6) can rescue the pollen defects in osmkk4 mutants, confirming that OsMPK6 functions downstream of OsMKK4 in this pathway. Genetic crosses also demonstrated that the MAPK cascade sporophyticly regulates pollen development. Our study reveals a novel function of rice MAPK cascade in plant male reproductive biology.

Keywords: MAPK cascade; degradation; pollen fertility; rice; tapetum.

MeSH terms

  • Fertility / genetics
  • Fertility / physiology
  • Flowers / genetics
  • Flowers / physiology
  • Gene Expression Regulation, Plant*
  • MAP Kinase Signaling System
  • Mitogen-Activated Protein Kinases* / genetics
  • Mitogen-Activated Protein Kinases* / metabolism
  • Mutation / genetics
  • Oryza* / enzymology
  • Oryza* / genetics
  • Oryza* / growth & development
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Pollen* / genetics
  • Pollen* / growth & development

Substances

  • Plant Proteins
  • Mitogen-Activated Protein Kinases