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Autophagy-mediated regulation of phytohormone metabolism during rice anther development.

ABSTRACT: Autophagy has recently been shown to be required for postmeiotic anther development including anther dehiscence, programmed cell death-mediated degradation of the tapetum and pollen maturation in rice. Several phytohormones are known to play essential roles during male reproductive development including pollen maturation. However, the relationship between phytohormone metabolism and autophagy in plant reproductive development is unknown. We here comprehensively analyzed the effect of autophagy disruption on phytohormone contents in rice anthers at the flowering stage, and found that endogenous levels of active-forms of gibberellins (GAs) and cytokinin, trans-zeatin, were significantly lower in the autophagy-defective mutant, Osatg7-1, than in the wild type. Treatment with GA₄ partially recovered maturation of the mutant pollens, but did not recover the limited anther dehiscence as well as sterility phenotype. These results suggest that autophagy affects metabolism and endogenous levels of GAs and cytokinin in rice anthers. Reduction in bioactive GAs in the autophagy-deficient mutant may partially explain the defects in pollen maturation of the autophagy-deficient mutant, but tapetal autophagy also plays other specific roles in fertilization.

SUBMITTER: Kurusu T

PROVIDER: S-EPMC5640179 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Autophagy-mediated regulation of phytohormone metabolism during rice anther development.

Kurusu Takamitsu T Koyano Tomoko T Kitahata Nobutaka N Kojima Mikiko M Hanamata Shigeru S Sakakibara Hitoshi H Kuchitsu Kazuyuki K

Plant signaling & behavior 20170905 9

Autophagy has recently been shown to be required for postmeiotic anther development including anther dehiscence, programmed cell death-mediated degradation of the tapetum and pollen maturation in rice. Several phytohormones are known to play essential roles during male reproductive development including pollen maturation. However, the relationship between phytohormone metabolism and autophagy in plant reproductive development is unknown. We here comprehensively analyzed the effect of autophagy d ...[more]

PMID: 28873038

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Project description:Background and aimsTapiscia sinensis (Tapisciaceae) is a functional androdioecious species with both male and hermaphroditic individuals, and fruit ripening overlaps with flowering in the hermaphroditic individuals. Pollen vitality was lower in the hermaphrodites than in the males. Anther development requires nutrients, and carbohydrates are the basic nutrients; abnormal carbohydrate metabolism will result in pollen abortion. The aim of this research was to gain insight into the relationship between carbohydrate metabolism and the weakening of the male function of hermaphroditic flowers in T. sinensis.MethodsObservation of morphology and microscopic and sub-microscopic structures was carried out. Sugar measurements and quantitative real-time PCR analysis were performed for the genes related to sugar metabolism and transport in the development of anthers in both males and hermaphrodites. The expression pattern of Cell wall invertase 2 (CWI2) and Sucrose transporter 2 (ST2) was explored by in situ hybridization.Key resultsAt the vacuolate microspore (VM) stage, polysaccharides accumulated in the connective tissue of the hermaphroditic anthers, and the levels of total soluble sugar, sucrose and starch in the hermaphroditic anthers were significantly lower than in the male anthers. Most of the hermaphroditic pollen grains were empty, with degradation of the cytoplasm, absence of an intine layer and defective exines. There was a significant differential expression between male and hermaphroditic flowers of several key genes that are involved in sugar metabolism, transport and intine development. CWI2 and ST2 were expressed in the tapetum and microspores. The expression of CWI2 was significantly lower in hermaphrodites than in the males.ConclusionsFruit ripening overlaps with flowering, leading to a severe reproductive burden on the hermaphroditic individuals. The hermaphroditic flowers regulating carbohydrate metabolism and transport to affect resources are biased towards the female function to ensure reproduction, causing a deficiency in resources for the development of pollen; thus, the pollen viability is lower. This makes it easier for males to invade the hermaphroditic population and form a functional androdioecious breeding system.

Project description:Gene expression throughout the reproductive process in rice (Oryza sativa) beginning with primordia development through pollination/fertilization to zygote formation was analyzed. We analyzed 25 stages/organs of rice reproductive development including early microsporogenesis stages with 57,381 probe sets, and identified around 26,000 expressed probe sets in each stage. Fine dissection of 25 reproductive stages/organs combined with detailed microarray profiling revealed dramatic, coordinated and finely tuned changes in gene expression. Decrease of expressed genes in the pollen maturation process was observed in a similar way with Arabidopsis and maize. An almost equal number of ab initio predicted genes and cloned genes appeared or disappeared coordinated with developmental stage progression. A large number of organ-/stage-specific genes were identified; notably 2,593 probe sets for developing anther, including 932 probe sets corresponding to ab initio predicted genes. Analysis of cell cycle-related genes revealed that several CDKs, cyclins and components of SCF E3 ubiquitin ligase complexes were expressed specifically in reproductive organs. Cell wall biosynthesis or degradation protein genes and transcription factor genes expressed specifically in reproductive stages were also newly identified. Rice genes homologous to reproduction-related genes in other plants showed expression profiles both consistent and inconsistent with their predicted functions. The rice reproductive expression atlas is likely to be the deepest and most comprehensive dataset available, indispensable for unraveling functions of many specific genes in plant reproductive processes that have not yet been thoroughly analyzed. Keywords: developmental stage comparison, tissue comparison, platform comparison Anther development of rice from hypodermal archesporial cells formation to tri-cellular mature pollens were divided into eight stages. Three or four biological replicates at each stage were analyzed with Affymetrix Rice Genome Array, and total number of samples in this series is 26.

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Autophagy-mediated regulation of phytohormone metabolism during rice anther development.

Publications

Autophagy-mediated regulation of phytohormone metabolism during rice anther development.

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