Yingxiang Wang
Changbin Chen
Gregory P. Copenhaver
Chung-Ju Rachel Wang- 1College of Life Sciences, South China Agricultural University, Guangzhou, China
- 2Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China
- 3School of Life Sciences, Arizona State University, Tempe, AZ, United States
- 4Department of Biology and the Integrative Program for Biological and Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, United States
- 5Lineberger Comprehensive Cancer Center, University of North Carolina School of Medicine, Chapel Hill, NC, United States
- 6Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
Editorial on the Research Topic
Meiosis in plants: sexual reproduction, genetic variation and crop improvement
Meiosis is essential for sexual reproduction and required for the formation of sperm and egg; its central events are the associations between homologous chromosomes (homologs), including pairing, synapsis, recombination and segregation. During recombination, the exchange of DNA between homologs results in new allelic combinations between the parents and offspring and among individual progeny (Wang and Copenhaver, 2018). This genetic variation is the foundation for biodiversity and speciation. The phenotypic diversity that results from genetic variation is also used to develop new elite traits during commercial plant and animal breeding practices. Thus, understanding the molecular mechanisms drive and regulate plant meiosis can accelerate crop improvement, and provide a theoretical foundation for the development and maintenance of new agricultural varieties.
Over the past three decades, molecular genetic studies have made great advances in understanding meiosis in plant species mainly by focusing on Arabidopsis, maize and rice. To improve our understanding of the potential applications of meiosis research in non-model plant or crop species, especially in polyploid plants, we organized this Research Topic which features seven original research articles covering five species including rice, wheat, allohexaploid Brassica, tomato, and Elymus. To present these findings in an accessible manner, we have organized them in to three themes: i) Molecular mechanism of meiotic recombination, ii) Meiosis in polyploid plants, and iii) Meiotic restitution induced by environmental stressors.
Molecular mechanism of meiotic recombination
Our Research Focus includes two papers that advance our understanding of the mechanisms that govern double-strand-break (DSB) and crossover (CO) formation. Meiotic recombination is initiated by the formation of DSBs that require multiple proteins including MEIOSIS INHIBITOR 4 (MEI4/REC24/PRD2) (Cole et al., 2010). PRD2 was first demonstrated to be required for plant meiotic DSB formation in Arabidopsis (De Muyt et al., 2009). Wang et al. identified rice PRD2 and demonstrated that it plays a conserved role in meiotic DSB formation in monocots (rice) and dicots (Arabidopsis), which diverged 140-150 Myr ago (Chaw et al., 2004). This study also provided evidence that OsPRD2 is dispensable for spindle assembly and organization, which is different from the previous finding in Arabidopsis.
FIDGETIN-LIKE-1 (FIGNL1) encodes a conserved AAA-ATPase that belongs to the FIDGETIN subfamily and acts later in recombination (Yuan and Chen, 2013). Arabidopsis has a single copy of FIGL1 that acts as an anti-crossover factor that limits class II CO formation, likely by influencing DMC1-mediated single strand invasion (Fernandes et al., 2018). Yang et al. identified the rice homolog FIGNL1 and demonstrated that, in addition to limiting class II CO formation, FIGNL1 is also required for limiting non-homologous chromosome associations during meiotic DSB repair. Moreover, FIGNL1 interacts with MEICA1 (meiotic chromosome association 1), which has a domain of unknown function (DUF4487). The chromosomal localization of FIGNL1 is dependent on synaptonemal complex assembly. Studying both of these the recombination-associated genes in rice has advanced our understanding of meiotic progression in plants, revealing both commonalities and differences.
Meiosis in polyploid plants
Our Research Topic includes four papers that examine mechanisms that regulate meiosis in allopolyploid plants. Polyploidization, or the duplication of whole chromosome sets, is a very common phenomenon in plants. The widespread presence of polyploidy across plant taxa is counterintuitive since multi-chromosomal interaction between homologous and homeologous chromosomes poses a risk to proper chromosome segregation. Hexaploid wheat (bread wheat, Triticum aestivum) has been an important experimental system for exploring this issue because of Pairing homeologous1 (Ph1), a complex locus that safeguards proper synapsis and crossing over between homologs (Sears, 1976). In T. aestivum the ZIP4 paralogue TaZIP4-B2 is located in the Ph1 locus and promotes CO formation between homologs by suppressing COs between homeologous chromosomes (Rey et al., 2017). Draeger et al. reported that three ZIP4 copies (TtZIP4-A1, TtZIP4-B1 and TtZIP4-B2) exist in Tetraploid wheat (pasta wheat, Triticum turgidum ssp. durum), and that disruption of both TtZIP4-A1/B1 genes results in a 76-78% reduction in COs, while mutation of all three genes leads to 95% reduction in COs, indicating that TtZIP4s are required for both Class I and II CO formation. In addition, TtZIP4-B2 was found to have a strong effect on synapsis in wheat, which is distinct to the previous findings of ZIP4 in Arabidopsis and rice.
DMC1 is a meiosis-specific recombinase with weak intrinsic ATPase activity, which is conserved in most eukaryotes (Xu et al., 2023). Interestingly, Draeger et al. found that, in the hexaploid wheat variety ‘Chinese Spring’, a mutation of the D-genome homeolog of DMC1 (TaDMC1-D1) causes a significant reduction of COs in a temperature responsive manner, exhibiting a more substantial change at low temperatures (13°C) compared with high temperatures (30°C). This finding not only reveals new information about how DMC1 is regulated in different species, but may also provide an important tool for improving wheat breeding and engineering resilience to climate change.
Artificially synthesized Brassica allohexaploids have superior stress resistance and high oilseed yield, but suffer from reduced fertility. Tian et al. used cytology and transcriptomics to investigate meiosis and pollen development in synthetic Brassica allohexaploids. Their results show that anther structure and tapetum development appears normal, but meiotic chromosome segregation is aberrant. Transcriptomic analyses showed that genes related to chromosome segregation were obviously downregulated in the synthetic Brassica allohexaploids, providing a potential explanation for the abnormal chromosome segregation.
Elymus nutans, a perennial grass and potential forage crop (Liu et al., 2022), is an allopolyploid with a StStYYHH (2n = 6x = 42) genome and is widely distributed in the Qinghai-Tibet Plateau of China. Populations of E. nutans have high levels of intergenomic translocations and chromosomal variations (Dou et al., 2017). As a result, E. nutans individuals that are heterozygous for chromosomal rearrangements often have meiotic defects. Liu et al. performed sequential fluorescence in situ hybridization (FISH) and genomic in situ hybridization (GISH) to examine the intra- and inter-genome chromosomal variations in E. nutans heterozytous plants. They observed that the meiotic chromosome abnormalities including bridges, fragments, unequal segregation, and lagging chromatids at various stages. In addition, this study also identified several paracentric inversions. This work highlights the utility of E. nutans as an important system for understanding chromosome structural variation in polyploid plants.
Meiotic restitution induced by environmental stressors
Rounding out our Research Focus, we have a study on the influence of heat stress on meiosis in tomato. Meiotic restitution occurs when one of the two divisions of meiosis is disrupted resulting in the formation of diploid spores. Meiotic restitution can result from genetic variants, but can also be influenced by external factors such as ambient temperature as has been observed in rose, Populus pseudosimonii, and Arabidopsis (De Storme and Geelen, 2013). Other environmental factors including drought, and high-UV have also been implicated in triggering abnormal meiosis, and meiotic restitution (Qi and Zhang, 2019). Schindfessel et al. reported that, in tomato, heat stress (>35°C) interferes with homologous chromosome synapsis, thus leading to the defects in meiotic recombination and chromosome segregation. Interestingly, they also find that heat stress has a role in converting meiotic divisions to “mitotic-like” divisions, a form of restitution, likely due to influence the spindle organization, which results in the formation of diploid pollen.
In summary, this Research Topic brings together recent findings, highlighting multiple non-model crops to improve our understanding of the molecular mechanisms of plant meiosis, and provide new insights into how meiosis works in polyploidy plants. These advances will be useful for efforts to engineer meiosis and recombination to enhance agriculture.
Author contributions
YW: Writing – original draft, Writing – review & editing. CC: Writing – original draft. GC: Writing – review & editing. CW: Writing – review & editing.
Funding
Work in the laboratory of YW was supported by grant from National Natural Science Foundation of China (31925005). Research in the laboratory of CC has been supported by the National Science Foundation (NSF-IOS-1546792 and NSF-IOS-2232948).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
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References
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Keywords: meiotic recombination, allopolyploid, double-strand-break, crossover, DMC1, PRD2, ZIP4, FIGNL1
Citation: Wang Y, Chen C, Copenhaver GP and Wang C-JR (2023) Editorial: Meiosis in plants: sexual reproduction, genetic variation and crop improvement. Front. Plant Sci. 14:1294591. doi: 10.3389/fpls.2023.1294591
Received: 15 September 2023; Accepted: 22 September 2023;
Published: 28 September 2023.
Edited and Reviewed by:
Simon Gilroy, University of Wisconsin-Madison, United StatesCopyright © 2023 Wang, Chen, Copenhaver and Wang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Yingxiang Wang, eXh3YW5nQHNjYXUuZWR1LmNu; Changbin Chen, Y2NoZW4zNDdAYXN1LmVkdQ==