Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize

Abstract

Common rust, caused by Puccinia sorghi, is a widespread and destructive disease of maize. The Rp1‐D gene confers resistance to the P. sorghi IN2 isolate, mediating a hypersensitive cell death response (HR). To identify differentially expressed genes (DEGs) and metabolites associated with the compatible (susceptible) interaction and with Rp1‐D‐mediated resistance in maize, we performed transcriptomics and targeted metabolome analyses of P. sorghi IN2‐infected leaves from the near‐isogenic lines H95 and H95:Rp1‐D, which differed for the presence of Rp1‐D. We observed up‐regulation of genes involved in the defence response and secondary metabolism, including the phenylpropanoid, flavonoid, and terpenoid pathways. Metabolome analyses confirmed that intermediates from several transcriptionally up‐regulated pathways accumulated during the defence response. We identified a common response in H95:Rp1‐D and H95 with an additional H95:Rp1‐D‐specific resistance response observed at early time points at both transcriptional and metabolic levels. To better understand the mechanisms underlying Rp1‐D‐mediated resistance, we inferred gene regulatory networks occurring in response to P. sorghi infection. A number of transcription factors including WRKY53, BHLH124, NKD1, BZIP84, and MYB100 were identified as potentially important signalling hubs in the resistance‐specific response. Overall, this study provides a novel and multifaceted understanding of the maize susceptible and resistance‐specific responses to P. sorghi.

Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

“…The homologs of these genes in different plant species also act in plant immunity (Coll et al, 2010;Senthil-Kumar et al, 2010;Gallego-Giraldo et al, 2011;Zeilmaker et al, 2015), suggesting the functional association between disease resistance and HR regulation. Recently, it was reported that the transcriptional responses triggered by Rp1-D21 are broadly similar to those triggered by its wild type (WT) counterpart Rp1-D, which is activated by Puccinia sorghi infection (Kim et al, 2021). The DEGs identified in Rp1-D21 are highly correlated with disease resistance; therefore, Rp1-D21 can be used as a quick and effective tool for exploring new HR regulation and disease resistance genes.…”

The maize ZmMIEL1 E3 ligase and ZmMYB83 transcription factor proteins interact and regulate the hypersensitive defence response

“…In Arabidopsis, the exaggerated HR induced in AtMYB30-overexpressing lines was suppressed by the loss of function of the acyl-ACP thioesterase FATB, which causes severe defects in the supply of fatty acids for VLCFA biosynthesis (Raffaele et al, 2008). In our study of the maize transcriptional response to P. sorghi, several VLCFA biosynthetic genes differentially accumulated in near-isogenic lines differing for induction of the defence response mediated by Rp1-D (Kim et al, 2021). We found that the transcript levels of four VLCFA biosynthetic genes that carried AtMYB30-specific binding sites in their promoters were down-regulated in plants in which ZmMYB83 expression was suppressed and up-regulated in plants in which ZmMIEL1 expression was suppressed (Figure 8a), as would be expected if ZmMIEL1/ZmMYB30 acts in a similar fashion to AtMIEL1/ AtMYB30.…”

“…Within these two groups the sequences were almost identical. Interrogating data from a separate RNA-Seq study (Kim et al, 2021), we noted that expression of ZmMIEL1 during the Rp1-D-mediated ETI response to P. sorghi was not induced significantly until the 120-hr postinoculation (hpi) timepoint. In contrast in a nearisogenic susceptible line without Rp1-D, ZmMIEL1 was induced early in the maize-P. sorghi interaction at 12 hpi but was induced less at 24 hpi and not at all at 120 hpi (Figure S6).…”

Omics-Facilitated Crop Improvement for Climate Resilience and Superior Nutritive Value

“…Besides, metabolomic profiling of soybean leaf tissues by GC-MS and LC-MS analyses revealed the role of phytochemical metabolism, as well as sugar and nitrogen metabolism in conferring tolerance to combined drought and heat stress conditions ( Das et al, 2017 ). Integrated metabolomic, transcriptomic and gene regulatory network analyses of common rust ( Puccinia sorghi ) resistance in maize identified a number of Rp1-D -mediated defense response metabolites (including chlorogenic acid, caffeic acid, ferulic acid, flavonoids, terpenoids, kauralexins and zealexins) and genes involved in SA biosynthesis (especially, calmodulin-binding protein 60G and systemic acquired resistance deficient 1, SARD 1; and several TFs such as WRKY53, BZIP84, NKD1, BHLH124 and MYB100) as potentially critical regulators of P. sorghi resistance in maize ( Kim S.B. et al, 2021 ).…”