Implementation of Epigenetic Variation in Sorghum Selection and Implications for Crop Resilience Breeding

Abstract

Crop resilience and yield stability are complex traits essential for food security. Sorghum bicolor is an important grain crop that shows promise for its natural resilience to drought and potential for marginal land production. We have developed sorghum lines in the Tx430 genetic background suppressed for MSH1 expression as a means of inducing de novo epigenetic variation, and have used these materials to evaluate changes in plant growth vigor. Plant crossing and selection in two distinct environments revealed features of phenotypic plasticity derived from MSH1 manipulation. Introduction of an epigenetic variation to an isogenic sorghum population, in the absence of selection, resulted in 10% yield increase under ideal field conditions and 20% increase under extreme low nitrogen conditions. However, incorporation of early-stage selection amplified these outcomes to 36% yield increase under ideal conditions and 64% increase under marginal field conditions. Interestingly, the best outcomes were derived by selecting mid-range performance early-generation lines rather than highest performing. Data also suggested that phenotypic plasticity derived from the epigenetic variation was non-uniform in its response to environmental variability but served to reduce genotype × environment interaction. The MSH1-derived growth vigor appeared to be associated with enhanced seedling root growth and altered expression of auxin response pathways, and plants showed evidence of cold tolerance, features consistent with observations made previously in Arabidopsis. These data imply that the MSH1 system is conserved across plant species, pointing to the value of parallel model plant studies to help devise effective plant selection strategies for epigenetic breeding in multiple crops.

Will epigenetics be a key player in crop breeding?

“…Following removal of the RNAi suppression via outcrossing and selection of transgene-null segregants, lines with stably enhanced growth and vigor can be identified. This has been documented in tomato (Yang et al, 2015), soybean [Glycine max L. (Merr)] (Raju et al, 2018), and sorghum (Sorghum bicolor L. Moench) (Ketumile et al, 2022). These results indicate that some epimutations/epialleles and epigenomic states that condition agriculturally-important traits are heritable and it is conceivable that they have played a wider role in crop breeding than previously known.…”

“…Furthermore, A. thaliana F 1 plants generated by crossing between epi-RIL and wild type parents showed enhanced vegetative growth (Dapp et al, 2015;Lauss et al, 2018). DNA methylation repatterning caused by msh1 resulted Tonosaki et al 10.3389/fpls.2022.958350 in enhanced growth in the F 4 generation of crosses between msh1 and wild type in A. thaliana (Virdi et al, 2015), and a similar phenomenon was observed in sorghum (Ketumile et al, 2022). These findings suggest epigenetic variation can potentially become sources for breeding high yielding crops.…”

“…While studies of the role of epigenetic inheritance in adaptation is by definition and interest largely focused on adaptation to a given stress or environmental change, in crop production it is of equal practical importance that the epigenetic changes may enhance progeny crop performance in production environments that are optimal or relatively non-stressful. Perhaps this is what has been demonstrated via the MSH1-RNAi approach of the Mackenzie group (Kundariya et al, 2020;Yang et al, 2020;Ketumile et al, 2022). In that approach, a form of metabolic stress is imposed via silencing of MSH1 using RNAi.…”

Epigenetic Changes Occurring in Plant Inbreeding

“…DNA methylation changes can additionally be generated using a variety of techniques. For example, DNA methylation patterns in crop plants can be influenced by using the MSH1 ( MutS Homolog1 ) gene suppression approach, using the RNAi mechanism [ 30 , 31 , 32 ]. In inbred lines of Sorghum bicolor , it is revealed that the epigenetic variability, induced by the MSH1 system, influenced plant yields and resistance.…”

“…The development of epiRIL in Arabidopsis also allowed the mapping of epigenetic loci of quantitative traits (epiQTL) [ 26 ], which enables the analysis of the role of the epigenetic variability in the regulation of agricultural properties. Due to the lack of DNA methylation mutants in crop plants [ 27 ], pharmacological strategies with DNA MTase inhibitors or the MSH1 system are used, which lead to changes in DNA methylation, affecting the yield and resistance of plants [ 28 , 29 , 30 , 31 , 32 ]. An example of such “epimutagenesis” is the development of the Oryza sativa line, resistant to Xanthomonas oryzae , after having been treated with 5-azacytidine [ 28 ].…”