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.

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Sorghum (Sorghum bicolor) is drought‐tolerant and has diverse germplasm for food, feed, forage and bioenergy. However, stalk diseases reduce quality and yield of biomass and grain, especially under drought. Previously, brown midrib (bmr) mutations in monolignol biosynthesis were shown to reduce lignin content and alter composition but were not more susceptible to stalk diseases than wild‐type lines. Recently characterized bmr mutations were shown to affect flavonoid biosynthesis (chalcone isomerase; bmr30‐1) or 1‐carbon metabolism (folylpolyglutamate synthase; bmr19‐1107, bmr19‐1168 and bmr19‐1937). Two other mutations, bmr29‐1 and bmr31‐1, have not yet been characterized. The six mutations were incorporated into elite genetic backgrounds (RTx430, BTx623 and BWheatland) to develop near‐isogenic lines containing each mutation. Using peduncle inoculations with Fusarium thapsinum and F. proliferatum (Fusarium stalk rot) and Macrophomina phaseolina (charcoal rot) under well‐watered conditions, most bmr lines were at least as resistant as the corresponding wild type, except for RTx430 bmr19‐1937 that had significantly longer mean lesion lengths when inoculated with M. phaseolina. Based on significantly reduced lesion lengths following inoculations with F. proliferatum and F. thapsinum, respectively, bmr29‐1 and bmr31‐1 lines were screened using basal stalk inoculations under well‐watered and water‐deficit conditions. The bmr lines were at least as resistant as the corresponding wild‐type lines. Wild‐type BTx623 was highly susceptible to M. phaseolina under water deficit, but near‐isogenic bmr29‐1 and bmr31‐1 lines had significantly shorter mean lesion lengths. Incorporation of these mutations can increase resistance to stalk pathogens in cultivar and hybrid development for feed, bioenergy and production of biomass‐based green chemicals.

Sweet sorghum [Sorghum bicolor (L.) Moench] lines M81-E and Colman were previously shown to differ in responses to Fusarium thapsinum and Macrophomina phaseolina, stalk rot pathogens that can reduce yields and quality of biomass and extracted sugars. Inoculated tissues were compared for transcriptomic, phenolic metabolite, and enzymatic activity during disease development 3 and 13 days after inoculation (DAI). At 13 DAI M81-E had shorter mean lesion lengths than Colman when inoculated with either pathogen. Transcripts encoding monolignol biosynthetic and modification enzymes were associated with transcriptional wound (control) responses of both lines at 3 DAI. Monolignol biosynthetic genes were differentially coexpressed with transcriptional activator SbMyb76 in all Colman inoculations, but only following M. phaseolina inoculation in M81-E, suggesting that SbMyb76 is associated with lignin biosynthesis during pathogen responses. In control inoculations, defense-related genes were expressed at higher levels in M81-E than Colman. Line, treatment, and timepoint differences observed in phenolic metabolite and enzyme activities did not account for observed differences in lesions. However, generalized additive models were able to relate metabolites, but not enzyme activities, to lesion length, for quantitatively modeling disease progression: in M81-E, but not Colman, sinapic acid levels positively predicted lesion length at 3 DAI when cell wall-bound syringic acid was low, soluble caffeic acid was high, and lactic acid was high, suggesting that sinapic acid may contribute to responses at 3 DAI. These results provide potential gene targets for development of sweet sorghum varieties with increased stalk rot resistance to ensure biomass and sugar quality.