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Anatomy and RNA-Seq reveal important gene pathways regulating sex differentiation in a functionally Androdioecious tree, Tapiscia sinensis.

ABSTRACT: BACKGROUND:Gametogenesis is a key step in the production of ovules or pollen in higher plants. The sex-determination aspects of gametogenesis have been well characterized in the model plant Arabidopsis. However, little is known about this process in androdioecious plants. Tapiscia sinensis Oliv. is a functionally androdioecious tree, with both male and hermaphroditic individuals. Hermaphroditic flowers (HFs) are female-fertile flowers that can produce functional pollen and set fruits. However, compared with male flowers (MFs), the pollen viability and number of pollen grains per flower are markedly reduced in HFs. MFs are female-sterile flowers that fail to set fruit and that eventually drop. RESULTS:Compared with HF, a notable cause of MF female sterility in T. sinensis is when the early gynoecium meristem is disrupted. During the early stage of HF development (stage 6), the ring meristem begins to form as a ridge around the center of the flower. At this stage, the internal fourth-whorl organ is stem-like rather than carpelloid in MF. A total of 52,945 unigenes were identified as transcribed in MF and HF. A number of differentially expressed genes (DEGs) and metabolic pathways were detected as involved in the development of the gynoecium, especially the ovule, carpel and style. At the early gynoecium development stage, DEGs were shown to function in the metabolic pathways regulating ethylene biosynthesis and signal transduction (upstream regulator), auxin, cytokinin transport and signalling, and sex determination (or flower meristem identity). CONCLUSIONS:Pathways for the female sterility model were initially proposed to shed light on the molecular mechanisms of gynoecium development at early stages in T. sinensis.

SUBMITTER: Xin GL

PROVIDER: S-EPMC6915933 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Anatomy and RNA-Seq reveal important gene pathways regulating sex differentiation in a functionally Androdioecious tree, Tapiscia sinensis.

Xin Gui-Liang GL Liu Jia-Qian JQ Liu Jia J Ren Xiao-Long XL Du Xiao-Min XM Liu Wen-Zhe WZ

BMC plant biology 20191216 1

<h4>Background</h4>Gametogenesis is a key step in the production of ovules or pollen in higher plants. The sex-determination aspects of gametogenesis have been well characterized in the model plant Arabidopsis. However, little is known about this process in androdioecious plants. Tapiscia sinensis Oliv. is a functionally androdioecious tree, with both male and hermaphroditic individuals. Hermaphroditic flowers (HFs) are female-fertile flowers that can produce functional pollen and set fruits. Ho ...[more]

PMID: 31842763

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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:Background and aimsThe phylogeography of plant species in sub-tropical China remains largely unclear. This study used Tapiscia sinensis, an endemic and endangered tree species widely but disjunctly distributed in sub-tropical China, as a model to reveal the patterns of genetic diversity and phylogeographical history of Tertiary relict plant species in this region. The implications of the results are discussed in relation to its conservation management.MethodsSamples were taken from 24 populations covering the natural geographical distribution of T. sinensis. Genetic structure was investigated by analysis of molecular variance (AMOVA) and spatial analysis of molecular variance (SAMOVA). Phylogenetic relationships among haplotypes were constructed with maximum parsimony and haplotype network methods. Historical population expansion events were tested with pairwise mismatch distribution analysis and neutrality tests. Species potential range was deduced by ecological niche modelling (ENM).Key resultsA low level of genetic diversity was detected at the population level. A high level of genetic differentiation and a significant phylogeographical structure were revealed. The mean divergence time of the haplotypes was approx. 1·33 million years ago. Recent range expansion in this species is suggested by a star-like haplotype network and by the results from the mismatch distribution analysis and neutrality tests.ConclusionsClimatic oscillations during the Pleistocene have had pronounced effects on the extant distribution of Tapiscia relative to the Last Glacial Maximum (LGM). Spatial patterns of molecular variation and ENM suggest that T. sinensis may have retreated in south-western and central China and colonized eastern China prior to the LGM. Multiple montane refugia for T. sinense existing during the LGM are inferred in central and western China. The populations adjacent to or within these refugia of T. sinense should be given high priority in the development of conservation policies and management strategies for this endangered species.

Dataset Information

Anatomy and RNA-Seq reveal important gene pathways regulating sex differentiation in a functionally Androdioecious tree, Tapiscia sinensis.

Publications

Anatomy and RNA-Seq reveal important gene pathways regulating sex differentiation in a functionally Androdioecious tree, Tapiscia sinensis.

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