The central circadian regulator CCA1 functions in Glycine max during defense to a root pathogen, regulating the expression of genes acting in effector triggered immunity (ETI) and cell wall metabolites

Authors: NIRAULA, PRAKASH - Mississippi State University; MCNEECE, BRANT - Mississippi State University; SHARMA, K - Mississippi State University; ALKHAROUF, NADIM - Towson University; LAWRENCE, KATHERINE - Auburn University; Klink, Vincent

Submitted to: Plant Physiology and Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/20/2022
Publication Date: 5/30/2022
Citation: Niraula, P.M., Mcneece, B.T., Sharma, K., Alkharouf, N.W., Lawrence, K.S., Klink, V.P. 2022. The central circadian regulator CCA1 functions in Glycine max during defense to a root pathogen, regulating the expression of genes acting in effector triggered immunity (ETI) and cell wall metabolites. Plant Physiology and Biochemistry. 185:198-220. https://doi.org/10.1016/j.plaphy.2022.05.028.
DOI: https://doi.org/10.1016/j.plaphy.2022.05.028

Interpretive Summary: Plant root cells undergoing a defense response to a parasitic pathogen have been collected by laser microdissection. Genes expressed specifically in those cells have been identified through a bioinformatics analysis performed at the genomic level . The expression of four of those genes leads to resistance to the parasitic pathogen. Experiments reveal that one of the four genes functions as a master regulatory switch, functioning to activate the expression of other defense genes. Bioinformatics analyses of 9 other genomes of plants that are important to global food production and three other genomes of significance, including sugar beet (Beta vulgaris), have identified related genes (homologs). The analyses have resulted in the identification of a conserved mechanism of plant defense that would be of importance to agriculture, generally. The experiments have identified genes that function in plant defense and are present, broadly in various agricultural crops of significance. Scientists or others interested in crop improvement, specifically to pathogen resistance, now have gene targets in hand for crop improvement. through breeding, engineering or other means.

Technical Abstract: Expression of the central circadian oscillator components CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), TIMING OF CAB1 (TOC1), GIGANTEA (GI) and CONSTANS (CO) occurs in Glycine max root cells (syncytia) parasitized by the nematode Heterodera glycines while undergoing defense, indicating a defense role. GmCCA1-1 mRNA levels in roots undergoing overexpression (OE) and RNA interference (RNAi) cycle through light (day)-dark (night) cycles, peaking in late day. An out of phase GmCCA1-1 expression pattern shifting by 12 hours exists in infected as compared to uninfected controls. The H. glycines-resistant G. max[Peking/PI 548402] transgenic controls exhibit out of phase expression 4 hours post infection (hpi), not consistently occurring in the H. glycines-susceptible G. max[Williams 82/PI 518671] until 56 hpi. GmCCA1-1 expression is observed to be reduced in infected GmCCA1-1-OE roots as compared to non-infected transgenic roots with no significant change observed among RNAi roots. However, the GmCCA1-1 expression in transgenic GmCCA1-1-OE roots is still higher than control and RNAi roots. Decreased GmCCA1-1 mRNA among infected roots shows the altered expression is targeted directly or indirectly by H. glycines. The gene expression of proven defense genes including 9 different mitogen activated protein kinases (MAPKs), NON-RACE SPECIFIC DISEASE RESISTANCE 1 (NDR1), RPM1-INTERACTING PROTEIN 4 (RIN4), and the secreted xyloglucan endotransglycosylase/hydrolase (XTH43) in GmCCA1-1-OE and GmCCA1-1-RNAi roots as compared to their controls reveal a significant role of GmCCA1 expression in roots undergoing defense to H. glycines parasitism. The observation that GmCCA1-1 regulates XTH43 expression links the central circadian oscillator to the functionality of the secretion system.