Cold Influences Male Reproductive Development in Plants: A Hazard to Fertility, but a Window for Evolution

Liu, Bing; Mo, Wenjuan; Zhang, Dabing; Storme, Nico De; Geelen, Danny

doi:10.1093/pcp/pcy209

Cited by 26 publications

(23 citation statements)

References 139 publications

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“…Heat stress suppresses MR via compromised DSB formation MR in plants is sensitive to variations of environmental temperature (Bomblies et al, 2015;Liu et al, 2019;Modliszewski and Copenhaver, 2017). Lloyd et al proposed that MR rate of Arabidopsis under different temperature conditions within fertility-tolerable range displays a 'U-shape' pattern, in which both decreased (8°C) and increased (28°C) temperatures promote MR rate (Lloyd et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Environmental temperatures can affect multiple processes of meiotic cell division in plants (Liu et al, 2019;Morgan et al, 2017). In Arabidopsis, wheat, Populus and persimmon, temperature stresses affect formation and organization of spindle and/or phragmoplast during male meiosis, which results in meiotic restitution or aneuploid gametes (De Storme et al, 2012;Lei et al, 2020;Liu et al, 2018;Mai et al, 2019;Tang et al, 2011;Wang et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Ning

Liu

Wang

et al. 2020

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Meiotic recombination (MR) drives reciprocal exchange of genetic information which allows novel combination of alleles and contributes to genomic diversity of eukaryotes. In this study, we report that heat stress (36-38°C) over fertile threshold fully abolishes crossover occurrence by lowering the formation of SPO11-dependent double-strand breaks (DSBs) in Arabidopsis. The high temperature partially suppresses chromosome fragmentation in the rad51 and syn1 mutants by reducing DSB formation. In addition, we found that although the SYN1-mediated formation of chromosome axis is not influenced by the high temperature, ASY1-associated axial element of synaptonemal complex (SC) is partially compromised, and the ZYP1-dependent central element of axis is severely disrupted, indicating that homology synapsis is another prominent target of high temperature. Besides, we observed that the loading of recombinase DMC1 on chromatin is significantly reduced by high temperatures, suggesting that heat stress interferes with DMC1-dependent MR. Moreover, we found that the numbers of DSB and DMC1 keep stable within a limited range of temperature increase, while decrease when the DSB-processing system reaches threshold to heat. Furthermore, transcriptome study revealed a universal variation of the expression of meiotic genes under low (4°C) and high (32°C) temperatures, suggesting that temperature may influence MR by modulating the transcription of MR-related factors. We also found that the landscape of 5-methylcytosine (5mC) was altered under high temperatures, suggesting that environmental temperature may influence the distribution of MR via reshaped DNA methylation status of chromatin. Taken together, our findings provide evidence shedding light on how environment temperatures influence MR in Arabidopsis.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Ning

Liu

Wang

et al. 2020

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“…In turn, this simplification allows for the production of multiple different genome-wide CO maps with relatively little effort. Although it has long been known that many environmental factors influence CO rates, such as temperature, water stress, salinity, and pathogen stress 45,46 , the genetic mechanisms underlying this sensitivity have not been well characterized. We expect that our approach will greatly aid research in this area, as it is expected to make it feasible to directly compare CO maps generated from many different genotypes or environments.…”

Section: Discussionmentioning

confidence: 99%

Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination

et al. 2019

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Meiotic crossovers (COs) ensure proper chromosome segregation and redistribute the genetic variation that is transmitted to the next generation. Large populations and the demand for genome-wide, fine-scale resolution challenge existing methods for CO identification. Taking advantage of linked-read sequencing, we develop a highly efficient method for genome-wide identification of COs at kilobase resolution in pooled recombinants. We first test this method using a pool of Arabidopsis F2 recombinants, and recapitulate results obtained from the same plants using individual whole-genome sequencing. By applying this method to a pool of pollen DNA from an F1 plant, we establish a highly accurate CO landscape without generating or sequencing a single recombinant plant. The simplicity of this approach enables the simultaneous generation and analysis of multiple CO landscapes, accelerating the pace at which mechanisms for the regulation of recombination can be elucidated through efficient comparisons of genotypic and environmental effects on recombination.

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“…Temperature was believed to be the main factor affecting L.g.hexapetala fruitfulness and fertility (Dandelot et al, 2005). Indeed, increases or decreases in temperature after flower induction in some other plant species may deteriorate the production of viable male gametes and cause male sterility (Liu, Mo, Zhang, De Storme, & Geelen, 2019;Santiago & Sharkey, 2019). In France, fruitful populations were initially observed in the Atlantic zone, while fruitless populations were found in the Mediterranean zone, hypothesizing a climate effect on the reproductive success of L.g.hexapetala (Dandelot et al, 2005).…”

Section: No Environmental And/or Climate Factors Are Involved In the mentioning

confidence: 99%

Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive aquatic plant

Lemus¹,

Bozec²,

Harang³

et al. 2020

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SummaryFruitfulness and fertility are important components of sexual reproductive success in plants, and often depends on environmental conditions and reproductive systems. For invasive plants, fruitfulness and fertility control their ecological success and adaptation in invaded ecosystems. We studied which factors bring about fruitfulness and fertility in invasive populations of the aquatic plant Ludwigia grandiflora subsp. hexapetala.We analysed fruitfulness and fertility of 37 populations growing under variable climatic conditions in Western Europe, and sub-sampled fruitful and fruitless populations grown in common controlled conditions. We carried out self- and cross-pollinations and measured their floral biometrics.Environmental conditions, and temperature in particular, did not affect fruitfulness and fertility in-situ or in common controlled environments. Hand-pollinations resulted in fruit production by individuals sampled from fruitless populations when pollen came from fruitful populations, and by individuals sampled from fruitful populations whatever the origin of pollen. Floral biometrics evidenced the existence of two floral morphs that overlapped with fruitfulness, and individual incompatibility.Our results rebutted the hypothesis that environmental conditions control fruitfulness and fertility in these invasive populations. We instead found that fruit and seed production were controlled by a reproductive system involving a self-incompatible approach herkogamous morph and a self-compatible reverse herkogamous morph. We assessed the floral morphs distribution worldwide of fruitless and fruitful native and invasive populations that matched our results at larger scale. Our results may constitute the first evidence of a possible heteromorphic self-incompatible system in Ludwigia populations and in Onagraceae phylogeny. It calls for further investigations on reproductive systems in this plant family. Finally, the observation that the self-incompatible morph seemed to be the world most invasive morph in this species tackles our understanding of biological and ecological conditions for invasiveness.Synthesis. Our study showed that fruitfulness and fertility in the aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala depend on a self-incompatibility system coinciding with two floral morphs, rather than environmental conditions and limitations. These new explanations on the sexual success of Ludwigia invasive populations will help defining new predictions about its worldwide spreads and ecological success, and will help reappraising future management plans.

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Cold Influences Male Reproductive Development in Plants: A Hazard to Fertility, but a Window for Evolution

Cited by 26 publications

References 139 publications

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination

Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive aquatic plant

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