Identification and verification of genes related to pollen development and male sterility induced by high temperature in the thermo-sensitive genic male sterile wheat line

Abstract Background: Environment-sensitive genic male sterility is of vital importance to hybrid vigor in crop production and breeding, therefore, it is meaningful to identify and study the function of the genes related to pollen development and male sterility, which still not fully understanding currently. In this study, Yanzhan 4110S, a new thermo-sensitive genic male sterility (TGMS) wheat line, and its near isogenic line Yanzhan 4110 were carried out cytological features observation, bioinformatics analysis to investgate the abortion state and identified the genes involved in pollen development which have fertility regulation function. Barely stripe mosaic virus-induced gene silencing was used to verify the genes function.Results: Cytological analysis showed pollen abortion event of Yanzhan 4110S occur at the later uninucleate stage (Lun) under higher temperature induction (day/night temperatures of 22 °C/20 °C), when the anthers were collected and assessed for transcriptomic profiling through high-throughput sequencing. We then in-depth analyzed the differentially expressed genes (DEGs) by Gene Ontology, Kyoto Encyclopedia of Genes and Genomes, the results showed that the occurrence of Yanzhan 4110S male-sterility most likely related to metabolic pathway, including phenylpropanoid biosynthesis in the biosynthesis of other secondary metabolites, starch and sucrose metabolism in carbohydrate metabolism, carbon fixation in photosynthetic organisms as well as carbon metabolism in energy metabolism. The weighted gene co-expression network analysis in the transcriptome profiles further identified some hub genes, where the key genes involved in those pathways were intersection between the unique DEGs of Yanzhan 4110S in anther and hub genes, totally 228 genes, which were highly related to pollen development including TaMut11 and TaSF3. Moreover, further verification through barely stripe mosaic virus-induced gene silencing elucidated that the silencing of TaMut11 and TaSF3 caused pollen abortion, finally resulting in the declination of fertility. So, the genes TaMut11 and TaSF3 are related to fertility conversion of Yanzhan 4110S.Conclusion: Through comparative transcriptome bioinformatics analysis, the genes TaMut11 and TaSF3 associated with pollen development and male sterility induced by high temperature were identified in Yanzhan 4110S, and verificated by barely stripe mosaic virus-induced gene silencing. These findings provided researching the abortive mechanism in environment-sensitive genic male sterility wheat.

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Increased expression of the MALE STERILITY1 transcription factor gene results in temperature-sensitive male sterility in barley

Journal of Experimental Botany ◽

10.1093/jxb/eraa382 ◽

2020 ◽

Vol 71 (20) ◽

pp. 6328-6339

Author(s):

José Fernández-Gómez ◽

Behzad Talle ◽

Zoe A Wilson

Keyword(s):

Transcription Factor ◽

Male Sterility ◽

Pollen Development ◽

Breeding Systems ◽

Hybrid Breeding ◽

Temperature Sensitive ◽

Hybrid Vigour ◽

Male Sterile ◽

The Impact

Abstract Understanding the control of fertility is critical for crop yield and breeding; this is particularly important for hybrid breeding to capitalize upon the resultant hybrid vigour. Different hybrid breeding systems have been adopted; however, these are challenging and crop specific. Mutants with environmentally reversible fertility offer valuable opportunities for hybrid breeding. The barley HvMS1 gene encodes a PHD-finger transcription factor that is expressed in the anther tapetum, which is essential for pollen development and causes complete male sterility when overexpressed in barley. This male sterility is due at least in part to indehiscent anthers resulting from incomplete tapetum degeneration, failure of anther opening, and sticky pollen under normal growth conditions (15 °C). However, dehiscence and fertility are restored when plants are grown at temperatures >20 °C, or when transferred to >20 °C during flowering prior to pollen mitosis I, with transfer at later stages unable to rescue fertility in vivo. As far as we are aware, this is the first report of thermosensitive male sterility in barley. This offers opportunities to understand the impact of temperature on pollen development and potential applications for environmentally switchable hybrid breeding systems; it also provides a ‘female’ male-sterile breeding tool that does not need emasculation to facilitate backcrossing.

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Phenotype characterisation and analysis of expression patterns of genes related mainly to carbohydrate metabolism and sporopollenin in male-sterile anthers induced by high temperature in wheat (Triticum aestivum)

Crop and Pasture Science ◽

10.1071/cp18034 ◽

2018 ◽

Vol 69 (5) ◽

pp. 469 ◽

Cited By ~ 4

Author(s):

Hongzhan Liu ◽

Junsheng Wang ◽

Chaoqiong Li ◽

Lin Qiao ◽

Xueqin Wang ◽

...

Keyword(s):

Triticum Aestivum ◽

High Temperature ◽

Male Sterility ◽

Carbohydrate Metabolism ◽

Higher Plants ◽

Expression Patterns ◽

Triticum Aestivum L ◽

Male Sterile ◽

Tetrad Stage ◽

Expression Levels

Male reproductive development in higher plants is highly sensitive to various stressors, including high temperature (HT). In this study, physiological male-sterile plants of wheat (Triticum aestivum L.) were established using HT induction. The physiological changes and expression levels of genes mainly related to carbohydrate metabolism and sporopollenin in male-sterile processes were studied by using biological techniques, including iodine–potassium iodide staining, paraffin sectioning, scanning electron microscopy (SEM) and fluorescent quantitative analysis. Results of paraffin sectioning and SEM revealed that parts of HT male-sterile anthers, including the epidermis and tapetum, were remarkably different from those of normal anthers. The expression levels of TaSUT1, TaSUT2, IVR1 and IVR5 were significantly lower than of normal anthers at the early microspore and trinucleate stages. The RAFTIN1 and TaMS26 genes may contribute to biosynthesis and proper ‘fixation’ of sporopollenin in the development of pollen wall; however, their expression levels were significantly higher at the early tetrad stage and early microspore stage in HT sterile anthers. The recently cloned MS1 gene was expressed at the early tetrad and early microspore stages but not at the trinucleate stage. Moreover, this gene showed extremely significant, high expression in HT sterile anthers compared with normal anthers. These results demonstrate that HT induction of wheat male sterility is probably related to the expression of genes related to carbohydrate metabolism and sporopollenin metabolism. This provides a theoretical basis and technological approach for further studies on the mechanisms of HT induction of male sterility.

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Comparative analysis of anther development in natural populations indicate premature degradation of sporogenous tissue as a cause of male sterility in Gaultheria fragrantissima

10.1101/368886 ◽

2018 ◽

Author(s):

Wympher Langstang ◽

Eros Kharshiing ◽

Nagulan Venugopal

Keyword(s):

Comparative Analysis ◽

Male Sterility ◽

Pollen Development ◽

Natural Populations ◽

Anther Development ◽

Abnormal Development ◽

Male Sterile ◽

Male Sterile Line ◽

Sporogenous Tissue

AbstractGaultheria fragrantissima Wall. (Ericaceae) is a gynodioecious species having both hermaphrodite and male sterile plants. In this study, we present a comparative analysis of the different stages of anther development in naturally occuring hermaphrodite and male sterile populations of G. fragrantissima found in Meghalaya, India. While hermaphrodite flowers had well developed anther lobes, the male sterile flowers formed a white unorganized mass of tissues with a tuft of hairy outgrowth at the tip of the stamens. Histological analyses of progressive anther development in both the lines indicate an abnormal development of the sporogenous tissue in the developing anthers in the male steril line. While anther development in the hermaphrodite line was of the dicotyledonous type, the anthers of male sterile line showed progressive degradation of the sporogenous tissues and wall layers. Pollen development was also disrupted in male sterile line resulting in distorted pollen due to the irregular projection of exine wall. Our results suggest that premature degradation of the sporogenous tissues during anther development determines male sterility in G. fragrantissima.

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

10.1101/088526 ◽

2016 ◽

Author(s):

Gonul Dundar ◽

Zhenhua Shao ◽

Nahoko Higashitani ◽

Mami Kikuta ◽

Masanori Izumi ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Cell Death ◽

High Temperature ◽

Pollen Development ◽

Anther Wall ◽

List Type ◽

Male Sterile ◽

Cellular Processes ◽

Cellular Components ◽

Plant Pollen

AbstractAutophagy is one of the cellular processes that break down cellular components during senescence, starvation, and stress. The susceptibility of plant pollen development to high-temperature (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 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.HighlightsIn 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 HT-caused abortion of tapetal program cell death.

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Use of RNAi With OsMYB76R as a Reporter for Candidate Genes Can Efficiently Create and Verify Gametophytic Male Sterility in Rice

Frontiers in Plant Science ◽

10.3389/fpls.2021.728193 ◽

2021 ◽

Vol 12 ◽

Author(s):

Yun Chen ◽

Wenping Zhu ◽

Shudan Shi ◽

Lina Wu ◽

Shuanglin Du ◽

...

Keyword(s):

Male Sterility ◽

Pollen Development ◽

Low Cost ◽

Mutation Screening ◽

Accurate Method ◽

Anthocyanin Synthesis ◽

Acid Oxidase ◽

Male Sterile ◽

Oxidase Gene ◽

Genetic Characteristics

Gametophytic male sterility (GMS) plays an important role in the study of pollen development and seed propagation of recessive nuclear male sterile lines insensitive to the environmental conditions in hybrid rice breeding. Since the inherent phenotypic and genetic characteristics of GMS, it is very difficult to find and identify the GMS mutants. However, due to the abundance of gene transcription data, a large number of pollen-specific genes have been found, and most of them may be associated with GMS. To promote the study of these genes in pollen development and heterosis utilization, in this study, an easy and efficient method of creating and identifying GMS was established using RNAi and OsMYB76R as a reporter. First, the OsC1/OsMYB76 gene involved in anthocyanin synthesis was modified, and we have validated that the modified OsMYB76R is workable as the same as the pre-modified OsMYB76 gene. Then, the ascorbic acid oxidase gene OsPTD1 was downregulated using RNAi, driven by its own promoter that resulted in abnormal pollen tube growth. Finally, the RNAi elements were linked with OsMYB76R and transformed into an osmyb76 mutant, and the distortion of purple color segregation was found in T1 and F1 generations. This indicates that the OsPTD1 GMS was prepared successfully. Compared to current methods, there are several advantages to this method. First, time is saved in material preparation, as one generation less needs to be compared than in the conventional method, and mutation screening can be avoided. In addition, for identification, the cost is lower; PCR, electrophoresis, and other processes are not needed; and no expensive chemicals or instruments are required. Finally, the results are more accurate, with much lower background effects, and no damage to the plant. The result is an easy, efficient, low-cost, and accurate method of preparing and identifying GMS genes.

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Inheritance of thermo-photoperiod sensitive male sterility in wheat

Australian Journal of Agricultural Research ◽

10.1071/ar05161 ◽

2006 ◽

Vol 57 (2) ◽

pp. 187 ◽

Cited By ~ 5

Author(s):

Rui-Xing Guo ◽

Dong-Fa Sun ◽

Xun-Dong Cheng ◽

De-Fu Rong ◽

Chengdao Li

Keyword(s):

High Temperature ◽

Low Temperature ◽

Male Sterility ◽

Common Wheat ◽

Hybrid Seed Production ◽

Male Sterile ◽

Male Sterile Line ◽

Wheat Varieties ◽

Sowing Dates ◽

Recessive Genes

The fertility of a wheat male sterile line 337S was investigated in 4 consecutive years with 18 different sowing dates. Line 337S showed high sterility under both short daylength/low temperature and long daylength/high temperature during ear development. It has 2 time windows to be used as a male sterile line for hybrid seed production. Its fertility rate can be >50% with suitable sowing time; thus, it can be self-maintained as a male sterile line. Line 337S was reciprocally crossed with 7 common wheat varieties and the fertility of their F1, F2, and BC1 hybrids was investigated at different sowing dates. The results showed that recessive nuclear genes controlled male sterility in 337S and no cytoplasmic effect was observed. All common wheat varieties were able to restore its fertility. The male sterility was controlled by a pair of recessive genes under short daylength/low temperature, but was governed by 2 pairs of recessive genes under long daylength/high temperature. This novel male sterile line provides a new tool for using heterosis in wheat.

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QTL mapping of male sterility‐related traits in a photoperiod and temperature‐sensitive genic male sterile wheat line BS366

Plant Breeding ◽

10.1111/pbr.12811 ◽

2020 ◽

Vol 139 (3) ◽

pp. 498-507 ◽

Cited By ~ 2

Author(s):

Shao‐hua Yuan ◽

Jian‐fang Bai ◽

Hao‐yu Guo ◽

Wen‐jing Duan ◽

Zi‐han Liu ◽

...

Keyword(s):

Qtl Mapping ◽

Male Sterility ◽

Temperature Sensitive ◽

Wheat Line ◽

Male Sterile

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The Mitochondrial Genome Assembly of Fennel (Foeniculum vulgare) Reveals Two Different atp6 Gene Sequences in Cytoplasmic Male Sterile Accessions

International Journal of Molecular Sciences ◽

10.3390/ijms21134664 ◽

2020 ◽

Vol 21 (13) ◽

pp. 4664

Author(s):

Fabio Palumbo ◽

Nicola Vitulo ◽

Alessandro Vannozzi ◽

Gabriele Magon ◽

Gianni Barcaccia

Keyword(s):

Male Sterility ◽

Single Molecule ◽

Pollen Development ◽

Energy Demand ◽

Nuclear Dna ◽

High Energy ◽

Male Sterile ◽

Functional Protein ◽

Foeniculum Vulgare ◽

F1 Hybrid

Cytoplasmic male sterility (CMS) has always aroused interest among researchers and breeders, being a valuable resource widely exploited not only to breed F1 hybrid varieties but also to investigate genes that control stamen and pollen development. With the aim of identifying candidate genes for CMS in fennel, we adopted an effective strategy relying on the comparison between mitochondrial genomes (mtDNA) of both fertile and sterile genotypes. mtDNA raw reads derived from a CMS genotype were assembled in a single molecule (296,483 bp), while a draft mtDNA assembly (166,124 nucleotides, 94 contigs) was performed using male fertile sample (MF) sequences. From their annotation and alignment, two atp6-like sequences were identified. atp6−, the putative mutant copy with a 300 bp truncation at the 5’-end, was found only in the mtDNA of CMS samples, while the wild type copy (atp6+) was detected only in the MF mtDNA. Further analyses (i.e., reads mapping and Sanger sequencing), revealed an atp6+ copy also in CMS samples, probably in the nuclear DNA. However, qPCRs performed on different tissues proved that, despite its availability, atp6+ is expressed only in MF samples, while apt6− mRNA was always detected in CMS individuals. In the light of these findings, the energy deficiency model could explain the pollen deficiency observed in male sterile flower. atp6− could represent a gene whose mRNA is translated into a not-fully functional protein leading to suboptimal ATP production that guarantees essential cellular processes but not a high energy demand process such as pollen development. Our study provides novel insights into the fennel mtDNA genome and its atp6 genes, and paves the way for further studies aimed at understanding their functional roles in the determination of male sterility.

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