Pathogen and drought stress affect cell wall and phytohormone signaling to shape host responses in a sorghum COMT bmr12 mutant

Authors: Khasin, Maya; Bernhardson, Lois; O`Neill, Patrick; Palmer, Nathan - Nate; Scully, Erin; Sattler, Scott; Funnell-Harris, Deanna

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/27/2021
Publication Date: 8/21/2021
Publication URL: https://handle.nal.usda.gov/10113/7482179
Citation: Khasin, M., Bernhardson, L.F., O'Neill, P.M., Palmer, N.A., Scully, E.D., Sattler, S.E., Funnell-Harris, D.L. 2021. Pathogen and drought stress affect cell wall and phytohormone signaling to shape host responses in a sorghum COMT bmr12 mutant. Biomed Central (BMC) Plant Biology. 21:391. https://doi.org/10.1186/s12870-021-03149-5.
DOI: https://doi.org/10.1186/s12870-021-03149-5

Interpretive Summary: Sorghum is a drought-tolerant biomass crop grown in the United States and worldwide for animal feed, and as a feedstock for biofuels. Lignin provides strength to plant cell walls and is a major component of plant biomass. Plants can alter the amount of lignin in their cell walls based on environmental conditions, such as drought and disease. The amount and structure of this compound impacts digestibility, which effects its uses for livestock feed, fuel, and other products. Brown midrib (bmr) mutants in sorghum have reduced amounts of lignin, which makes them more usable for feed and fuels, but it may make them more vulnerable to disease under drought. Stalk rots are diseases that can seriously reduce biomass yields, in part due to lodging, which impacts the ability to harvest. However, the natural drought tolerance of sorghum enables the study of how these plants react to stalk rot diseases, Fusarium stalk rot and charcoal rot, under drought conditions compared to well-watered conditions. This study found that brown midrib mutant plants bmr6 and bmr12 are not more susceptible to these diseases under either well-watered or drought conditions. In fact, bmr12 had reduced disease under drought than when the plants were well-watered. In bmr12 plants, there is activation of defense pathways under drought conditions, which might explain their ability to withstand stalk diseases. These results show that there is a possible fundamental connection between plant cell wall structure and the ability to survive disease under drought; this information could be used when researching other

Technical Abstract: Background As effects of global climate change intensify, the interaction of biotic and abiotic stresses increasingly threatens current agricultural practices. The secondary cell wall is a vanguard of resistance to these stresses. Fusarium thapsinum (Fusarium stalk rot) and Macrophomina phaseolina (charcoal rot) cause internal damage to the stalks of the drought tolerant C4 grass, sorghum (Sorghum bicolor (L.) Moench), resulting in reduced transpiration, reduced photosynthesis, and increased lodging, severely reducing yields. Drought can magnify these losses. Two null alleles in monolignol biosynthesis of sorghum (brown midrib 6-ref, bmr6-ref; cinnamyl alcohol dehydrogenase, CAD; and bmr12-ref; caffeic acid O-methyltransferase, COMT) were used to investigate the interaction of water limitation with F. thapsinum or M. phaseolina infection. Results The bmr12 plants inoculated with either of these pathogens had increased levels of salicylic acid (SA) and jasmonic acid (JA) across both watering conditions and significantly reduced lesion sizes under water limitation compared to adequate watering, which suggested that drought may prime induction of pathogen resistance. RNA-Seq analysis revealed coexpressed genes associated with pathogen infection. The defense response included phytohormone signal transduction pathways, primary and secondary cell wall biosynthetic genes, and genes encoding components of the spliceosome and proteasome. Conclusion Alterations in the composition of the secondary cell wall affect immunity by influencing phenolic composition and phytohormone signaling, leading to the action of defense pathways. Some of these pathways appear to be activated or enhanced by drought. Secondary metabolite biosynthesis and modification in SA and JA signal transduction may be involved in priming a stronger defense response in water-limited bmr12 plants.