Dataset Information

Transcriptomic Analysis Reveals a Comprehensive Calcium- and Phytohormone-Dominated Signaling Response in Leymus chinensis Self-Incompatibility.

ABSTRACT: Sheepgrass (Leymus chinensis (Trin.) Tzvel.) is an economically and ecologically important forage in the grass family. Self-incompatibility (SI) limits its seed production due to the low seed-setting rate after self-pollination. However, investigations into the molecular mechanisms of sheepgrass SI are lacking. Therefore, microscopic observation of pollen germination and pollen tube growth, as well as transcriptomic analyses of pistils after self- and cross-pollination, were performed. The results indicated that pollen tube growth was rapidly inhibited from 10 to 30 min after self-pollination and subsequently stopped but preceded normally after cross-pollination. Time course comparative transcriptomics revealed different transcriptome dynamics between self- and cross-pollination. A pool of SI-related signaling genes and pathways was generated, including genes related to calcium (Ca²⁺) signaling, protein phosphorylation, plant hormone, reactive oxygen species (ROS), nitric oxide (NO), cytoskeleton, and programmed cell death (PCD). A putative SI response molecular model in sheepgrass was presented. The model shows that SI may trigger a comprehensive calcium- and phytohormone-dominated signaling cascade and activate PCD, which may explain the rapid inhibition of self-pollen tube growth as observed by cytological analyses. These results provided new insight into the molecular mechanisms of sheepgrass (grass family) SI.

SUBMITTER: Chen S

PROVIDER: S-EPMC6539167 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Transcriptomic Analysis Reveals a Comprehensive Calcium- and Phytohormone-Dominated Signaling Response in <i>Leymus chinensis</i> Self-Incompatibility.

Chen Shuangyan S Jia Junting J Cheng Liqin L Zhao Pincang P Qi Dongmei D Yang Weiguang W Liu Hui H Dong Xiaobing X Li Xiaoxia X Liu Gongshe G

International journal of molecular sciences 20190513 9

Sheepgrass (<i>Leymus chinensis</i> (Trin.) Tzvel.) is an economically and ecologically important forage in the grass family. Self-incompatibility (SI) limits its seed production due to the low seed-setting rate after self-pollination. However, investigations into the molecular mechanisms of sheepgrass SI are lacking. Therefore, microscopic observation of pollen germination and pollen tube growth, as well as transcriptomic analyses of pistils after self- and cross-pollination, were performed. Th ...[more]

PMID: 31085987

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Project description:BackgroundMany Poaceae species show a gametophytic self-incompatibility (GSI) system, which is controlled by at least two independent and multiallelic loci, S and Z. Until currently, the gene products for S and Z were unknown. Grass SI plant stigmas discriminate between pollen grains that land on its surface and support compatible pollen tube growth and penetration into the stigma, whereas recognizing incompatible pollen and thus inhibiting pollination behaviors. Leymus chinensis (Trin.) Tzvel. (sheepgrass) is a Poaceae SI species. A comprehensive analysis of sheepgrass stigma transcriptome may provide valuable information for understanding the mechanism of pollen-stigma interactions and grass SI.ResultsThe transcript abundance profiles of mature stigmas, mature ovaries and leaves were examined using high-throughput next generation sequencing technology. A comparative transcriptomic analysis of these tissues identified 1,025 specifically or preferentially expressed genes in sheepgrass stigmas. These genes contained a significant proportion of genes predicted to function in cell-cell communication and signal transduction. We identified 111 putative transcription factors (TFs) genes and the most abundant groups were MYB, C2H2, C3H, FAR1, MADS. Comparative analysis of the sheepgrass, rice and Arabidopsis stigma-specific or preferential datasets showed broad similarities and some differences in the proportion of genes in the Gene Ontology (GO) functional categories. Potential SI candidate genes identified in other grasses were also detected in the sheepgrass stigma-specific or preferential dataset. Quantitative real-time PCR experiments validated the expression pattern of stigma preferential genes including homologous grass SI candidate genes.ConclusionsThis study represents the first large-scale investigation of gene expression in the stigmas of an SI grass species. We uncovered many notable genes that are potentially involved in pollen-stigma interactions and SI mechanisms, including genes encoding receptor-like protein kinases (RLK), CBL (calcineurin B-like proteins) interacting protein kinases, calcium-dependent protein kinase, expansins, pectinesterase, peroxidases and various transcription factors. The availability of a pool of stigma-specific or preferential genes for L. chinensis offers an opportunity to elucidate the mechanisms of SI in Poaceae.

Project description:BackgroundLeymus chinensis (L. chinensis) is a perennial native forage grass widely distributed in the steppe of Inner Mongolia as the dominant species. Calcium (Ca) is an essential mineral element important for plant adaptation to the growth environment. Ca limitation was previously shown to strongly inhibit Arabidopsis (Arabidopsis thaliana) seedling growth and disrupt plasma membrane stability and selectivity, increasing fluid-phase-based endocytosis and contents of all major membrane lipids.ResultsIn this study, we investigated the significance of Ca for L. chinensis growth and membrane stability relative to Arabidopsis. Our results showed that Ca limitation did not affect L. chinensis seedling growth and endocytosis in roots. Moreover, the plasma membrane maintained high selectivity. The lipid phosphatidylcholine (PC): phosphatidylethanolamine (PE) ratio, an indicator of the membrane stability, was five times higher in L. chinensis than in Arabidopsis. Furthermore, in L. chinensis, Ca limitation did not affect the content of any major lipid types, decreased malondialdehyde (MDA) content, and increased superoxide dismutase (SOD) activity, showing an opposite pattern to that in Arabidopsis. L. chinensis roots accumulated higher contents of PC, phosphatidylinositol (PI), monogalactosyldiacylglycerol (MGDG), phosphatidylglycerol (PG), cardiolipin (CL), digalactosyldiacylglycerol (DGDG), and lysophosphatidylcholine (LPC) but less phosphatidylethanolamine (PE), diacylglycerol (DAG), triacylglycerolv (TAG), phosphatidylserine (PS), lysobisphosphatidic acids (LPAs), lysophosphatidylethanolamine (LPE), and lysophosphatidylserine (LPS) than Arabidopsis roots. Moreover, we detected 31 and 66 unique lipids in L. chinensis and Arabidopsis, respectively.ConclusionsThis study revealed that L. chinensis roots have unique membrane lipid composition that was not sensitive to Ca limitation, which might contribute to the wider natural distribution of this species.

Dataset Information

Transcriptomic Analysis Reveals a Comprehensive Calcium- and Phytohormone-Dominated Signaling Response in Leymus chinensis Self-Incompatibility.

Publications

Transcriptomic Analysis Reveals a Comprehensive Calcium- and Phytohormone-Dominated Signaling Response in <i>Leymus chinensis</i> Self-Incompatibility.

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