Impact of Autophagy on Gene Expression and Tapetal Programmed Cell Death During Pollen Development in Rice

Abstract

Autophagy has recently been shown to be required for tapetal programmed cell death (PCD) and pollen maturation in rice. A transcriptional regulatory network is also known to play a key role in the progression of tapetal PCD. However, the relationship between the gene regulatory network and autophagy in rice anther development is mostly unknown. Here, we comprehensively analyzed the effect of autophagy disruption on gene expression profile during the tapetal PCD in rice anther development using high-throughput RNA sequencing. Expression of thousands of genes, including specific transcription factors and several proteases required for tapetal degradation, fluctuated synchronously at specific stages during tapetal PCD progression in the wild-type anthers, while this fluctuation showed significant delay in the autophagy-deficient mutant Osatg7-1. Moreover, gene ontology enrichment analysis in combination with self-organizing map clustering as well as pathway analysis revealed that the expression patterns of a variety of organelle-related genes as well as genes involved in carbohydrate/lipid metabolism were affected in the Osatg7-1 mutant during pollen maturation. These results suggest that autophagy is required for proper regulation of gene expression and quality control of organelles and timely progression of tapetal PCD during rice pollen development.

Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap

“…Recently, a rice (Oryza sativa) atg7 mutant has been reported to show defects in pollen maturation and anther dehiscence resulting in reduced male fertility 34 . The rice phenotype might be caused by an autophagy-dependent differentiation and metabolic reprogramming in the anther tapetum, which would imply divergent species-specific roles of autophagy in this tissue.…”

“…Our finding that the execution of distal LRC PCD is not dependent on autophagy is in line with the observation that autophagy-defective mutants in Arabidopsis do not show detrimental defects in other developmental processes involving PCD, such as xylem tracheary element differentiation, seed development, or tapetum degeneration 13 . Recently, a rice ( Oryza sativa ) atg7 mutant has been reported to show defects in pollen maturation and anther dehiscence resulting in reduced male fertility 34 . The rice phenotype might be caused by an autophagy-dependent differentiation and metabolic reprogramming in the anther tapetum, which would imply divergent species-specific roles of autophagy in this tissue.…”

Programmed Cell Death (PCD) in Plant: Molecular Mechanism, Regulation, and Cellular Dysfunction in Response to Development and Stress

“…Pollen ROS mediate [14] Osatg7-1 mediate [15] ROS mediate [16] PERSISTENT TAPETAL CELL2 mediate [17] AtLSD1 deathosome mediate [18] Female floral buds AMC9, MeGI, BAG5, AifA, and HSP70 mediate [19] Female gametophyte Auxin efflux [20] Fruit Ca 2+ -dependent nuclease [21] Double Fertilization ROS mediate [22] Vegetative cells PrpS-PrsS modulate PCD vegetative cells [23] Zygotic Embryogenesis - [24] Somatic Embryogenesis K + ATP channel activity [25] Phenol-storing cells [26] Embryonic Suspensor Cell - [27] Table 1.…”

Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

“…For example, the Gibberellins (GAs)-deficient mutant Osatg7-1 is male sterile characterized by significantly reduced GA contents and defective microsporogenesis. The exogenous application of GAs cannot restore pollen fertility ( Kurusu et al, 2017 ; Hanamata et al, 2020 ). The different behavior of different phytohormone male sterile mutants suggests that the application of technology will largely depend on the underlying genetic cause of male sterility, hence can be applied to the selected genes, which demands enhanced understandings.…”