Meiotic crossover reduction by virus‐induced gene silencing enables the efficient generation of chromosome substitution lines and reverse breeding in <i>Arabidopsis thaliana</i>

Calvo‐Baltanás, Vanesa; Wijnen, Cris L; Yang, Chao; Lukhovitskaya, Nina I.; Snoo, C. Bastiaan de; Hohenwarter, Linus; Keurentjes, J.J.B.; Jong, Hans de; Schnittger, Arp; Wijnker, Erik

doi:10.1111/tpj.14990

Cited by 6 publications

(13 citation statements)

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“…Having one or a few CO would still lead to low production of CO-free gametes but will also increase the production of gametes with low CO numbers, which would prove useful for reverse breeding. This strategy was recently validated by downregulating Arabidopsis MSH5 gene expression through VIGS ( Calvo-Baltanas et al, 2020 ). Furthermore, VIGS has the additional advantage of allowing transient downregulation and thus avoids integration of a stable transgene in the genome, which is a strong concern for breeders.…”

Section: How Can We Remodel Meiosis For Crop Improvement?mentioning

confidence: 99%

Rewiring Meiosis for Crop Improvement

2021

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Meiosis is a specialized cell division that contributes to halve the genome content and reshuffle allelic combinations between generations in sexually reproducing eukaryotes. During meiosis, a large number of programmed DNA double-strand breaks (DSBs) are formed throughout the genome. Repair of meiotic DSBs facilitates the pairing of homologs and forms crossovers which are the reciprocal exchange of genetic information between chromosomes. Meiotic recombination also influences centromere organization and is essential for proper chromosome segregation. Accordingly, meiotic recombination drives genome evolution and is a powerful tool for breeders to create new varieties important to food security. Modifying meiotic recombination has the potential to accelerate plant breeding but it can also have detrimental effects on plant performance by breaking beneficial genetic linkages. Therefore, it is essential to gain a better understanding of these processes in order to develop novel strategies to facilitate plant breeding. Recent progress in targeted recombination technologies, chromosome engineering, and an increasing knowledge in the control of meiotic chromosome segregation has significantly increased our ability to manipulate meiosis. In this review, we summarize the latest findings and technologies on meiosis in plants. We also highlight recent attempts and future directions to manipulate crossover events and control the meiotic division process in a breeding perspective.

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Section: How Can We Remodel Meiosis For Crop Improvement?mentioning

confidence: 99%

Rewiring Meiosis for Crop Improvement

2021

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“…This was successfully used in wheat for both basic and applicative researches ( Bennypaul et al, 2012 ; Lee et al, 2015 ). Moreover, VIGS treatment were successfully applied to manipulate meiotic-specific processes in wheat and Arabidopsis ( Bhullar et al, 2014 ; Calvo-Baltanás et al, 2020 ; Desjardins et al, 2020b ).…”

Section: Introductionmentioning

confidence: 99%

Redistribution of Meiotic Crossovers Along Wheat Chromosomes by Virus-Induced Gene Silencing

et al. 2021

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Meiotic recombination is the main driver of genetic diversity in wheat breeding. The rate and location of crossover (CO) events are regulated by genetic and epigenetic factors. In wheat, most COs occur in subtelomeric regions but are rare in centromeric and pericentric areas. The aim of this work was to increase COs in both “hot” and “cold” chromosomal locations. We used Virus-Induced gene Silencing (VIGS) to downregulate the expression of recombination-suppressing genes XRCC2 and FANCM and of epigenetic maintenance genes MET1 and DDM1 during meiosis. VIGS suppresses genes in a dominant, transient and non-transgenic manner, which is convenient in wheat, a hard-to-transform polyploid. F1 hybrids of a cross between two tetraploid lines whose genome was fully sequenced (wild emmer and durum wheat), were infected with a VIGS vector ∼ 2 weeks before meiosis. Recombination was measured in F2 seedlings derived from F1-infected plants and non-infected controls. We found significant up and down-regulation of CO rates along subtelomeric regions as a result of silencing either MET1, DDM1 or XRCC2 during meiosis. In addition, we found up to 93% increase in COs in XRCC2-VIGS treatment in the pericentric regions of some chromosomes. Silencing FANCM showed no effect on CO. Overall, we show that CO distribution was affected by VIGS treatments rather than the total number of COs which did not change. We conclude that transient silencing of specific genes during meiosis can be used as a simple, fast and non-transgenic strategy to improve breeding abilities in specific chromosomal regions.

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“…It first decomposes traits by generating numerous homozygous lines from a given heterozygous plant, from which desirable phenotypic traits can be selected in combination or in part. The crossing of complementing homozygous lines for the desired traits yields a hybrid which resembles fully or partially the genome of the starting heterozygous (Wijnker et al, 2012;Calvo-Baltanás et al, 2020; Figure 4A).…”

Section: Reverse Breeding Application To Hybrid Necrosis and Heterosismentioning

confidence: 99%

“…The technical application of reverse breeding demands two conditions: (1) the downregulation of meiotic recombination to preserve the two parental haplotypes that were combined in the starting hybrid and (2) the regeneration of the resulting gametes as a double-haploid (hereafter DH) population to obtain homozygous lines (Dirks et al, 2009;Wijnker et al, 2012; Figure 4). To date, reverse breeding has been shown in the model organism A. thaliana through complete and partial crossover (hereafter CO) suppression by silencing genes essential for meiotic recombination (Wijnker et al, 2012;Calvo-Baltanás et al, 2020). In the latest design, a meiotic gene required for about 83-87% of the total number of COs, MSH5 (MUT-S HOMOLOG 5; Higgins et al, 2004Higgins et al, , 2008Lu et al, 2008), was silenced in a wild-type hybrid using virus-induced gene silencing (VIGS; Calvo-Baltanás et al, 2020).…”

Section: Reverse Breeding Application To Hybrid Necrosis and Heterosismentioning

confidence: 99%

“…To date, reverse breeding has been shown in the model organism A. thaliana through complete and partial crossover (hereafter CO) suppression by silencing genes essential for meiotic recombination (Wijnker et al, 2012;Calvo-Baltanás et al, 2020). In the latest design, a meiotic gene required for about 83-87% of the total number of COs, MSH5 (MUT-S HOMOLOG 5; Higgins et al, 2004Higgins et al, , 2008Lu et al, 2008), was silenced in a wild-type hybrid using virus-induced gene silencing (VIGS; Calvo-Baltanás et al, 2020). The silencing of MSH5 resulted in non-recombinant and low-recombinant chromosomes segregating to gametes.…”

Section: Reverse Breeding Application To Hybrid Necrosis and Heterosismentioning

confidence: 99%

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Hybrid Incompatibility of the Plant Immune System: An Opposite Force to Heterosis Equilibrating Hybrid Performances

2021

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Hybridization is a core element in modern rice breeding as beneficial combinations of two parental genomes often result in the expression of heterosis. On the contrary, genetic incompatibility between parents can manifest as hybrid necrosis, which leads to tissue necrosis accompanied by compromised growth and/or reduced reproductive success. Genetic and molecular studies of hybrid necrosis in numerous plant species revealed that such self-destructing symptoms in most cases are attributed to autoimmunity: plant immune responses are inadvertently activated in the absence of pathogenic invasion. Autoimmunity in hybrids predominantly occurs due to a conflict involving a member of the major plant immune receptor family, the nucleotide-binding domain and leucine-rich repeat containing protein (NLR; formerly known as NBS-LRR). NLR genes are associated with disease resistance traits, and recent population datasets reveal tremendous diversity in this class of immune receptors. Cases of hybrid necrosis involving highly polymorphic NLRs as major causes suggest that diversified R gene repertoires found in different lineages would require a compatible immune match for hybridization, which is a prerequisite to ensure increased fitness in the resulting hybrids. In this review, we overview recent genetic and molecular findings on hybrid necrosis in multiple plant species to provide an insight on how the trade-off between growth and immunity is equilibrated to affect hybrid performances. We also revisit the cases of hybrid weakness in which immune system components are found or implicated to play a causative role. Based on our understanding on the trade-off, we propose that the immune system incompatibility in plants might play an opposite force to restrict the expression of heterosis in hybrids. The antagonism is illustrated under the plant fitness equilibrium, in which the two extremes lead to either hybrid necrosis or heterosis. Practical proposition from the equilibrium model is that breeding efforts for combining enhanced disease resistance and high yield shall be achieved by balancing the two forces. Reverse breeding toward utilizing genomic data centered on immune components is proposed as a strategy to generate elite hybrids with balanced immunity and growth.

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Meiotic crossover reduction by virus‐induced gene silencing enables the efficient generation of chromosome substitution lines and reverse breeding in Arabidopsis thaliana

Cited by 6 publications

References 83 publications

Rewiring Meiosis for Crop Improvement

Rewiring Meiosis for Crop Improvement

Redistribution of Meiotic Crossovers Along Wheat Chromosomes by Virus-Induced Gene Silencing

Hybrid Incompatibility of the Plant Immune System: An Opposite Force to Heterosis Equilibrating Hybrid Performances

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