MSH1-Induced Non-Genetic Variation Provides a Source of Phenotypic Diversity in Sorghum bicolor

Santamaria, Roberto De la Rosa; Shao, Mon‐Ray; Wang, Guomei; Niño-Liu, D.; Kundariya, Hardik; Wamboldt, Yashitola; Dweikat, İsmail; Mackenzie, Sally A.

doi:10.1371/journal.pone.0108407

Cited by 34 publications

(24 citation statements)

References 26 publications

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“…To investigate the potential of msh1 ‐derived vigour in epi‐lines of soybean, assess inheritance and determine the longevity of enhanced growth behaviour through self‐pollination, we performed reciprocal crosses of msh1 memory lines with wild‐type Thorne (Figure S4). Plants in the F 1 generation were restored to the normal phenotype, ruling out cytoplasmic genetic changes for the msh1 memory phenotype (de la Rosa Santamaria et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…Recent studies have shown that crossing msh1 memory lines to their isogenic wild‐type counterpart can influence growth vigour in Arabidopsis , sorghum and tomato (de la Rosa Santamaria et al ., ; Virdi et al ., ; Yang et al ., ). To investigate the potential of msh1 ‐derived vigour in epi‐lines of soybean, assess inheritance and determine the longevity of enhanced growth behaviour through self‐pollination, we performed reciprocal crosses of msh1 memory lines with wild‐type Thorne (Figure S4).…”

Section: Resultsmentioning

confidence: 98%

“…Previous studies have shown the influence of MSH1 perturbation for altering growth in Arabidopsis , sorghum and tomato (de la Rosa Santamaria et al ., ; Virdi et al ., ; Yang et al ., ). The present study exploits epigenetic variation induced by MSH1 perturbation in soybean to develop epi‐lines that displayed an increase in seed yield from selected F 4 and F 5 families, subsiding by the F 6 generation, under large‐scale field conditions.…”

Section: Discussionmentioning

confidence: 98%

“…The altered phenotypes are somewhat attenuated but stable after segregation of the RNAi transgene, producing msh1 ‘memory’. In sorghum, crossing msh1 memory lines with isogenic wild type gives rise to enhanced vigour phenotypes that appear to respond to selection in small‐scale studies (de la Rosa Santamaria et al ., ). In tomato, MSH1‐ derived vigour phenotypes are heritable in glasshouse and field conditions, graft transmissible and obviated by treatment with 5‐azacytidine, further implicating DNA methylation in this phenomenon (Yang et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…RNAi suppression of MSH1 in monocot and dicot species produces an identical range of developmental phenotypes (de la Rosa Santamaria et al ., ; Xu et al ., ; Yang et al ., ). The altered phenotypes are somewhat attenuated but stable after segregation of the RNAi transgene, producing msh1 ‘memory’.…”

Section: Introductionmentioning

confidence: 99%

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An epigenetic breeding system in soybean for increased yield and stability

Raju

Shao

Sanchez

et al. 2018

Plant Biotechnology Journal

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SummaryEpigenetic variation has been associated with a wide range of adaptive phenotypes in plants, but there exist few direct means for exploiting this variation. RNAi suppression of the plant‐specific gene, MutS HOMOLOG1 (MSH1), in multiple plant species produces a range of developmental changes accompanied by modulation of defence, phytohormone and abiotic stress response pathways along with methylome repatterning. This msh1‐conditioned developmental reprogramming is retained independent of transgene segregation, giving rise to transgene‐null ‘memory’ effects. An isogenic memory line crossed to wild type produces progeny families displaying increased variation in adaptive traits that respond to selection. This study investigates amenability of the MSH1 system for inducing agronomically valuable epigenetic variation in soybean. We developed MSH1 epi‐populations by crossing with msh1‐acquired soybean memory lines. Derived soybean epi‐lines showed increase in variance for multiple yield‐related traits including pods per plant, seed weight and maturity time in both glasshouse and field trials. Selected epi‐F2:4 and epi‐F2:5 lines showed an increase in seed yield over wild type. By epi‐F2:6, we observed a return of MSH1‐derived enhanced growth back to wild‐type levels. Epi‐populations also showed evidence of reduced epitype‐by‐environment (e × E) interaction, indicating higher yield stability. Transcript profiling of epi‐lines identified putative signatures of enhanced growth behaviour across generations. Genes related to cell cycle, abscisic acid biosynthesis and auxin response, particularly SMALL AUXIN UP RNAs (SAURs), were differentially expressed in epi‐F2:4 lines that showed increased yield when compared to epi‐F2:6. These data support the potential of MSH1‐derived epigenetic variation in plant breeding for enhanced yield and yield stability.

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Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

An epigenetic breeding system in soybean for increased yield and stability

Raju

Shao

Sanchez

et al. 2018

Plant Biotechnology Journal

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Parental effects and provisioning under drought and low phosphorus stress in common bean

Lorts

Lynch

Brown

2019

Food and Energy Security

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Low soil fertility and drought are primary constraints for crop production and food security in many developing nations. Since smallholder farmers often collect seed for the next year's crop from plants grown with abiotic stress, it is important to understand how progeny from a stressed parental environment perform when they are grown under similar stresses. This study investigates the impact of a low phosphorus (P) or drought parental environment on progeny seed and root traits in common bean (Phaseolus vulgaris), with the intention of distinguishing impacts of reduced parental provisioning from adaptive responses. Greenhouse, field, and seedling experiments were used to evaluate seed, seedling, and mature root phenotypes in progeny from stressed and nonstressed parental conditions. In addition, progeny from different positions within the pod and pod developmental times were evaluated since they are expected to vary in parental provisioning. Seeds from the peduncular position in the pod had less individual seed weight, fewer basal roots, reduced root dry weight, and smaller taproot diameter than those from the stylar position. Progeny of some genotypes from drought‐stressed parents had smaller individual seed weight, fewer basal roots, less total seedling dry weight, shorter seedling basal roots, and smaller basal root diameters. Progeny of some genotypes from a low P parental environment had smaller individual seed P concentration, fewer shoot‐borne roots, and greater basal root whorl number. Progeny from drought‐stressed parents, progeny from a low P parental environment, and seeds from the peduncular position had root phenotypes that were likely to be related to less parental provisioning. Possible adaptive parental effects were found in both parental drought and parental low P studies. Adequate seed provision under stress merits consideration as a selection target in crop breeding for stressful environments.

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Epigenomic plasticity of Arabidopsis msh1 mutants under prolonged cold stress

et al. 2018

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Dynamic transcriptional and epigenetic changes enable rapid adaptive benefit to environmental fluctuations. However, the underlying mechanisms and the extent to which this occurs are not well known. MutS Homolog 1 (MSH1) mutants cause heritable developmental phenotypes accompanied by modulation of defense, phytohormone, stress‐response, and circadian rhythm genes, as well as heritable changes in DNA methylation patterns. Consistent with gene expression changes, msh1 mutants display enhanced tolerance for abiotic stress including drought and salt stress, while showing increased susceptibility to freezing temperatures. Despite changes in defense and biotic stress‐response genes, msh1 mutants showed increasing susceptibility to the bacterial pathogen Pseudomonas syringae. Our results suggest that chronic cold and low light stress (10°C, 150 μmol m−2 s−1) influences non‐CG methylation to a greater degree in msh1 mutants compared to wild‐type Col‐0. Furthermore, CHG changes are more closely pericentromeric, whereas CHH changes are generally more dispersed. This increased variation in non‐CG methylation pattern does not significantly affect the msh1‐derived enhanced growth behavior after mutants are crossed with isogenic wild type, reiterating the importance of CG methylation changes in msh1‐derived enhanced vigor. These results indicate that msh1methylome is hyper‐responsive to environmental stress in a manner distinct from the wild‐type response, but CG methylation changes are potentially responsible for growth vigor changes in the crossed progeny.

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MSH1-Induced Non-Genetic Variation Provides a Source of Phenotypic Diversity in Sorghum bicolor

Cited by 34 publications

References 26 publications

An epigenetic breeding system in soybean for increased yield and stability

An epigenetic breeding system in soybean for increased yield and stability

Parental effects and provisioning under drought and low phosphorus stress in common bean

Epigenomic plasticity of Arabidopsis msh1 mutants under prolonged cold stress

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