Tapetal-Delayed Programmed Cell Death (PCD) and Oxidative Stress-Induced Male Sterility of Aegilops uniaristata Cytoplasm in Wheat

Liu, Zihan; Shi, Xianglin; Li, Sha; Gan, Hu; Zhang, Lingli; Song, Xiyue

doi:10.3390/ijms19061708

Cited by 44 publications

(39 citation statements)

References 46 publications

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“…Ethylene-responsive transcription factor 115 and transcriptional factor basic helix-loop-helix 137 were both significantly upregulated in ogu CMS abortive buds. Therefore, our results were basically consistent with the results of previous studies [ 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 ], and the genes discovered related to energy metabolism, oxidation reduction process and phenylpropanoid biosynthesis, ethylene-responsive transcription factor 115 and transcriptional factor basic helix-loop-helix 137 may be important factors contributing to Broccoli ogu CMS pollen abortion and bud abortion. Further experiments are needed to elucidate the molecular mechanisms of these genes that lead to broccoli CMS and bud abortion.…”

Section: Discussionsupporting

confidence: 92%

“…Previous studies have shown that the genes involved in reactive oxygen species (ROS) homeostasis or antioxidative system balance may be important factors contributing to pollen abortion in cotton [ 46 ] and wheat [ 47 ]. Carbohydrate and energy metabolisms, oxidation-reduction system and phenylpropanoid metabolism pathways related genes may be important factor for CMS in soybean [ 48 ], rapeseed [ 49 ], cabbage [ 50 ], onion [ 51 ] and wheat [ 52 ].…”

Section: Discussionmentioning

confidence: 99%

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Normal and Abortive Buds Transcriptomic Profiling of Broccoli ogu Cytoplasmic Male Sterile Line and Its Maintainer

Shu

Zhang

Liu

et al. 2018

IJMS

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Bud abortion is the main factor affecting hybrid seeds’ yield during broccoli cross breeding when using ogura cytoplasmic male sterile (ogu CMS) lines. However, the genes associated with bud abortion are poorly understood. We applied RNA sequencing to analyze the transcriptomes of normal and abortive buds of broccoli maintainer and ogu CMS lines. Functional analysis showed that among the 54,753 annotated unigenes obtained, 74 and 21 differentially expressed genes in common were upregulated and downregulated in ogu CMS abortive buds compared with ogu CMS normal buds, maintainer normal, and abortive buds, respectively. Nineteen of the common differentially expressed genes were enriched by GO terms associated with glycosyl hydrolases, reactive oxygen species scavenging, inhibitor, and protein degradation. Ethylene-responsive transcription factor 115 and transcriptional factor basic helix-loop-helix 137 were significantly upregulated; transcription factors DUO1 and PosF21/RF2a/BZIP34 were downregulated in ogu CMS abortive buds compared with the other groups. Genes related to polygalacturonase metabolism, glycosyl hydrolases, oxidation reduction process, phenylalanine metabolism, and phenylpropanoid biosynthesis were significantly changed in ogu CMS abortive buds. Our results increase our understanding of bud abortion, provide a valuable resource for further functional characterization of ogu CMS during bud abortion, and will aid in future cross breeding of Brassica crops.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Normal and Abortive Buds Transcriptomic Profiling of Broccoli ogu Cytoplasmic Male Sterile Line and Its Maintainer

Shu

Zhang

Liu

et al. 2018

IJMS

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“…Likewise, higher ROS in atg2-1 and atg5-1 leaves was reported (Yoshimoto et al 2009). In addition, it has recently been shown that excess ROS generated in a cytoplasmicmale-sterile wheat line delayed tapetal PCD initiation and led to pollen abortion (Liu et al 2018), although the spatiotemporal regulation of ROS production is essential for tapetal PCD progression (Hu et al 2011;Xie et al 2014). Altogether, in addition to HT-induced ROS, over-accumulation of ROS in autophagy deficiency might strongly affect the spatiotemporal ROS signaling for tapetal PCD.…”

Section: Discussionmentioning

confidence: 99%

Autophagy Mitigates High-Temperature Injury in Pollen Development of Arabidopsis thaliana

Dündar

Shao

Higashitani

et al. 2016

Preprint

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Highlights In Arabidopsis, autophagy is not essential for completion of the life cycle under normal temperatures. High temperature (HT) stress induces autophagy in developing anther wall cells and microspores. Autophagy deficient atg mutants become almost completely male-sterile at moderate HT. Autophagy plays a role in tapetum degeneration and pollen development during HTcaused abortion of tapetal program cell death. AbstractAutophagy is one of the cellular processes that break down cellular components during senescence, starvation, and stress. The susceptibility of plant pollen development to hightemperature (HT) stress is well known, but the involvement of autophagy in HT injury is yet to be clarified. Here, we found that following transfer to 30 °C, all autophagy-deficient (atg) mutants (atg2-1, 5-1, 7-2, and 10-1) of Arabidopsis thaliana tested displayed visibly impaired pollen development and anther dehiscence. HT-induced male sterility significantly increased in the atg mutants, but the degree of HT-induced obstacles did not change between the wild type (WT) and mutants from the seedling stage to the bolting stage. Cytological analyses showed that 30 °C promoted autophagy and autolysosome formation in both anther wall cells and microspores in developing anthers of WT, but the atg5-1 mutant did not show completion of tapetum degeneration and microspore maturation. HT upregulated hydrogen peroxide and 2 dehydroascorbate reductase 1 production in both WT and atg5-1 anthers, but the basal levels were already higher in the mutant. HT repressed expression of UNDEAD and its regulator MYB80, which are required for tapetal programmed cell death (PCD) for proper pollen development. Taken together, our results suggest that autophagy functions in tapetum degeneration and pollen development during HT-caused tapetal PCD abortion.

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“…When stained with TTC and KI-I 2 , a number of pollen grains in anthers of NWMS1 were visible, but they did not have vitality (Figure 2f,g). In many cases, abnormal meiosis and premature tapetum degradation are direct factors causing pollen abortion in male sterility lines [43,44]. The pollen mother cells, meiosis, tapetum, and binucleate microspores of NWMS1 appeared normal (Figure 2a-d,j); later, the microspores collapsed and severe plasmolysis occurred (Figure 2e,j,k).…”

Section: Nwms1 Belongs To Binucleate Microspore Abortionmentioning

confidence: 99%

The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.)

Zhang

et al. 2019

IJMS

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Male sterility is a valuable trait for genetic research and production application of wheat (Triticum aestivum L.). NWMS1, a novel typical genic male sterility mutant, was obtained from Shengnong 1, mutagenized with ethyl methane sulfonate (EMS). Microstructure and ultrastructure observations of the anthers and microspores indicated that the pollen abortion of NWMS1 started at the early uninucleate microspore stage. Pollen grain collapse, plasmolysis, and absent starch grains were the three typical characteristics of the abnormal microspores. The anther transcriptomes of NWMS1 and its wild type Shengnong 1 were compared at the early anther development stage, pollen mother cell meiotic stage, and binucleate microspore stage. Several biological pathways clearly involved in abnormal anther development were identified, including protein processing in endoplasmic reticulum, starch and sucrose metabolism, lipid metabolism, and plant hormone signal transduction. There were 20 key genes involved in the abnormal anther development, screened out by weighted gene co-expression network analysis (WGCNA), including SKP1B, BIP5, KCS11, ADH3, BGLU6, and TIFY10B. The results indicated that the defect in starch and sucrose metabolism was the most important factor causing male sterility in NWMS1. Based on the experimental data, a primary molecular regulation model of abnormal anther and pollen developments in mutant NWMS1 was established. These results laid a solid foundation for further research on the molecular mechanism of wheat male sterility.which is one of the key ways to improve wheat yield [6]. Male sterility permits the production of hybrids on a commercial scale, relying on heterosis in crops, and can greatly increase selection efficiency of the yield [7]. In-depth understanding of the molecular mechanism of male sterility can help us to use it more effectively.Plant male sterility was first reported in the 18th century [8]. A large number of plant male sterility mutants have been reported over the past few decades. Male sterility includes cytoplasmic male sterility (CMS) controlled by mitochondrial genes coupled with nuclear genes, and genic male sterility (GMS) controlled by nuclear genes alone [9][10][11]. The pistils of the cytoplasmic male sterile lines and genic male sterile lines are normal, but their stamens are abnormal and cannot pollinate normally, which is due to stamen degeneration, pollen abortion, or functional sterility. GMS occurs in 216 species and 17 species crosses, while CMS occurs in more than 150 species and 271 species crosses [11][12][13]. Plant male sterility lines have been widely studied and applied successfully in many crops, such as maize (Zea mays), rice (Oryza sativa), soybean (Glycine max), and barley (Hordeum vulgare). Several wheat CMS lines have been studied and applied in production; however, commercial application is limited [14][15][16]. Possible applications of GMS in plant breeding have been reviewed and discussed for at least 30 years [17]. Up to now, only five GMS genes have been...

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Tapetal-Delayed Programmed Cell Death (PCD) and Oxidative Stress-Induced Male Sterility of Aegilops uniaristata Cytoplasm in Wheat

Cited by 44 publications

References 46 publications

Normal and Abortive Buds Transcriptomic Profiling of Broccoli ogu Cytoplasmic Male Sterile Line and Its Maintainer

Normal and Abortive Buds Transcriptomic Profiling of Broccoli ogu Cytoplasmic Male Sterile Line and Its Maintainer

Autophagy Mitigates High-Temperature Injury in Pollen Development of Arabidopsis thaliana

The Major Factors Causing the Microspore Abortion of Genic Male Sterile Mutant NWMS1 in Wheat (Triticum aestivum L.)

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