Phytochrome interacting factor 3 regulates pollen mitotic division through auxin signalling and sugar metabolism pathways in tomato

Abstract

The development of viable pollen determines male fertility, and is crucial for reproduction in flowering plants. Phytochrome interacting factor 3 (PIF3) acts as a central regulator of plant growth and development, but its relationship with pollen development has not been determined.Through genetic, histological and transcriptomic analyses, we identified an essential role for SlPIF3 in regulating tomato (Solanum lycopersicum) pollen development. Knocking out SlPIF3 using clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 resulted in pollen mitosis I arrest, and a failure to form viable pollen. We further demonstrated that both glutamate synthase 1 (SlGLT1) and cell wall invertase 9 (SlCWIN9), involved in auxin and sugar homeostasis, respectively, colocalised with SlPIF3 in the anthers and were directly regulated by SlPIF3. Knockout of either SlGLT1 or SlCWIN9 phenocopied the pollen phenotype of SlPIF3 knockout (Slpif3) lines.Slpif3 fertility was partially restored by exogenous auxin indole-3-acetic acid in a dosedependent manner.This study reveals a mechanism by which SlPIF3 regulates pollen development and highlights a new strategy for creating hormone-regulated genic male sterile lines for tomato hybrid seed production.

Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato

“…While many studies have identified the roles of sugars in pollen maturation and germination stages of pollen grain development, our study proposes similar roles of sugars during the early stages of pollen development, where maintaining optimum assimilation flow and sugar levels are crucial during microsporogenesis as well as microgametogenesis. In our recent study we identified that in the development of pollen in tomato mitotic division was also regulated through auxin signaling and sugar metabolism pathways [ 47 ]. Additionally, current studies show that starch and sugar are involved in pollen development, as reported in the articles ‘Deficiency of rice hexokinase HXK5 impairs synthesis and utilization of starch in pollen grains and causes male sterility’ [48] and ‘Comparative analysis of the transcriptome, methylome, and metabolome during pollen abortion of a seedless citrus mutant’ [ 49 ].…”

The bHLH1-DTX35/DFR module regulates pollen fertility by promoting flavonoid biosynthesis in Capsicum annuum L.

“…This may be the reason for the morphological changes in the epidermal cells of mutant anthers. In addition, recent studies have shown that the auxin signalling pathway regulates pollen mitotic division [ 36 ]. The expression levels of genes involved in plant hormone signal transduction were higher in mutant than WT anthers just prior to dehiscence.…”

Genic male and female sterility in vegetable crops

“…3b ). In tomato, SlMAPK4 (MITOGEN-ACTIVATED PROTEIN KINASE 4), SlMAPK20, and SlPIF3 (PHYTOCHROME INTERACTING FACTOR 3) have been demonstrated to play critical roles in microgametogenesis and specifically regulate post-meiotic pollen development through the sugar and auxin metabolism and signaling pathway [ 68 – 70 ]. Knockdown of SlMAPK20 or SlMAPK4 resulted in abnormally degraded cytoplasm at the binucleate stage of pollen development [ 68 , 69 ].…”

“…Knockdown of SlMAPK20 or SlMAPK4 resulted in abnormally degraded cytoplasm at the binucleate stage of pollen development [ 68 , 69 ]. SlPIF3 mediates the pollen mitosis I process by directly promoting the expression of both SlGLT1 ( GLUTAMATE SYNTHASE 1 ) and SlCWIN9 ( CELL WALL INVERTASE 9 ) in the tomato anther [ 70 ]. Knockout of SlGLT1 / SlCWIN9 phenocopied the defective bicellular pollen phenotypes of Slpif3 mutants [ 70 ].…”