Abnormal tapetum development and energy metabolism associated with sterility in SaNa-1A CMS of Brassica napus L.

Du, Kun; Xiao, Yuyue; Liu, Qier; Wu, Xinyue; Jiang, Jinjin; Wu, Jian; Fang, Yujie; Xiang, Yu‐Tao; Wang, Youping

doi:10.1007/s00299-019-02385-2

Cited by 21 publications

(24 citation statements)

References 58 publications

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“…In contrast, when ROS accumulation is increased in anthers such as in the isonuclear alloplasmic male sterile wheat ( Triticum aestivum ) that harbours Aegilops kotschyi cytoplasm, tapetum degradation was observed at the tetrad stage and was followed by pollen abortion (Liu, Shi, Li, Zhang, & Song, ). Increased anther accumulation of ROS was also recently seen in cytoplasmic male sterile Brassica napus along with deficiency in antioxidant enzyme system (Du et al, ). Overall, these studies show that a balanced and timed ROS accumulation is critical for pollen tube growth, tapetum integrity, and pollen viability.…”

Section: Effects Of Heat Stress On Male Reproductive Developmentmentioning

confidence: 76%

Pollen development at high temperature and role of carbon and nitrogen metabolites

Santiago

Sharkey

2019

Plant Cell & Environment

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Fruit and seed crop production heavily relies on successful stigma pollination, pollen tube growth, and fertilization of female gametes. These processes depend on production of viable pollen grains, a process sensitive to high-temperature stress. Therefore, rising global temperatures threaten worldwide crop production. Close observation of plant development shows that high-temperature stress causes morpho-anatomical changes in male reproductive tissues that contribute to reproductive failure. These changes include early tapetum degradation, anther indehiscence, and deformity of pollen grains, all of which are contributing factors to pollen fertility. At the molecular level, reactive oxygen species (ROS) accumulate when plants are subjected to high temperatures. ROS is a signalling molecule that can be beneficial or detrimental for plant cells depending on its balance with the endogenous cellular antioxidant system. Many metabolites have been linked with ROS over the years acting as direct scavengers or molecular stabilizers that promote antioxidant enzyme activity. This review highlights recent advances in research on anther and pollen development and how these might explain the aberrations seen during high-temperature stress; recent work on the role of nitrogen and carbon metabolites in anther and pollen development is discussed including their potential role at high temperature.

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Section: Effects Of Heat Stress On Male Reproductive Developmentmentioning

confidence: 76%

Pollen development at high temperature and role of carbon and nitrogen metabolites

Santiago

Sharkey

2019

Plant Cell & Environment

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“…Excessive ROS production and PCD abnormalities were also observed in the four-stage and early-nuclear stages of HL-CMS rice anthers [68]. Du et al [59] observed over-accumulation of ROS and signals of PCD in tetrads of SaNa-1A of B. napus.…”

Section: Discussionmentioning

confidence: 96%

“…In the present study, four of these five mitochondrial encoded genes were downregulated in msZY, and there was lower ATP content in young flower buds of msZY than in ZY (Figure 4). Abnormal energy metabolism or DEGs enriched in energy metabolism were observed in pol CMS [7], SaNa-1A CMS [59], and hau CMS [15]. Decreased ATP production was considered the reason for pollen abortion in transgenic tobacco [27] and rice [60].…”

Section: Discussionmentioning

confidence: 99%

Comparative Transcriptome Analysis Reveals the Potential Mechanism of Abortion in Tobacco sua-Cytoplasmic Male Sterility

Liu

Sun

et al. 2020

IJMS

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sua-CMS (cytoplasmic male sterility) is the only male sterile system in tobacco breeding, but the mechanism of abortion is unclear. Cytological characteristics show that abortion in the sua-CMS line msZY occurs before the differentiation of sporogenous cells. In this study, a comparative transcriptomic analysis was conducted on flower buds at the abortion stage of msZY and its male fertile control ZY. A total of 462 differentially expressed genes were identified in msZY and ZY, which were enriched via protein processing in the endoplasmic reticulum (ER), oxidative phosphorylation, photosynthesis, and circadian rhythm-plant by Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses. Most genes were downregulated in the ER stress pathway, heat-shock protein family, F1F0-ATPase encoding by the mitochondrial genome, and differentiation of stamens. Genes in the programmed cell death (PCD) pathway were upregulated in msZY. The transcriptome results were consistent with those of qRT-PCR. Ultrastructural and physiological analyses indicted active vacuole PCD and low ATP content in msZY young flower buds. We speculated that PCD and a deficiency in ATP synthesis are essential for the abortion of sua-CMS. This study reveals the potential mechanism of abortion of tobacco sua-CMS.

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“…Changes in atpA expression in the sesame CMS line reduced ATP biosynthesis in the mitochondria (Yang et al., 2008). In the SaNa‐1A CMS line of Brassica napus , ATP synthesis is inhibited by the abnormal structure and function of terminal oxidase caused by the sterility factor (Du et al., 2019). The fatty acid oxidation pathway is therefore initiated to satisfy the energy demand.…”

Section: Discussionmentioning

confidence: 99%

Comparative proteomic analysis of mitochondrial proteins from maize CMS‐C sterile, maintainer and restorer anthers

Zhang

Wang

et al. 2020

The Plant Genome

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The maize C system of cytoplasmic male sterility (CMS) and its fertility restoration gene Rf4 have been widely used for maize hybrid production; however, the underlying mechanism is still uncertain. The sterility factor functions in mitochondria, where it interacts directly or indirectly with the restorer. Mitoproteomics can capture all participants involved in CMS and restoration at the organelle level. In the present study, we identified and quantified anther mitochondrial proteins from CMS, maintainer and restorer lines. We obtained 14,528 unique peptides belonging to 3,369 proteins. Comparative analysis of 1840 high-confidence proteins revealed 68 were differentially accumulated proteins likely involved in CMS or its restoration within mitochondria. These proteins were mainly associated with fatty acid metabolism, amino acid metabolism and protein-processing pathways. These results suggest that an energy deficiency caused by the sterility factor hinders other proteins or protein complexes required for pollen development through nuclear-mitochondrial interaction. The restorer factor may boost the energy generation by activating alternative metabolic pathways and by improving the post-translation processing efficiency of proteins in energy-producing complexes to restore pollen fertility. Our findings may aid detailed molecular analysis and contribute to a better understanding of maize CMS-C restoration and sterility. 1 INTRODUCTION Plant cytoplasmic male sterility (CMS), the inability to produce functional pollen, is a widespread plant reproductive feature (Chen & Liu, 2014). This maternally inherited trait has Abbreviations: CMS, cytoplasm male sterility; DAP, differentially accumulated protein; iTRAQ, isobaric tags for relative and absolute quantification. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Abnormal tapetum development and energy metabolism associated with sterility in SaNa-1A CMS of Brassica napus L.

Cited by 21 publications

References 58 publications

Pollen development at high temperature and role of carbon and nitrogen metabolites

Pollen development at high temperature and role of carbon and nitrogen metabolites

Comparative Transcriptome Analysis Reveals the Potential Mechanism of Abortion in Tobacco sua-Cytoplasmic Male Sterility

Comparative proteomic analysis of mitochondrial proteins from maize CMS‐C sterile, maintainer and restorer anthers

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