Glycine max polygalacturonase inhibiting protein (PGIP) functions in the root to suppress Heterodera glycines parasitism

Authors: ACHARYA, SUDHA - Towson University; TROELL, HALLIE - Mississippi State University; BILLINGSLEY, REBECCA - Mississippi State University; LAWRENCE, KATHERINE - Auburn University; MCKIRGAN, DANIEL - Towson University; ALKHAROUF, NADIM - Towson University; Klink, Vincent

Submitted to: Plant Physiology and Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/19/2024
Publication Date: 5/24/2024
Citation: Acharya, S., Troell, H.A., Billingsley, R.L., Lawrence, K.S., Mckirgan, D.S., Alkharouf, N.W., Klink, V.P. 2024. Glycine max polygalacturonase inhibiting protein (PGIP) functions in the root to suppress Heterodera glycines parasitism. Plant Physiology and Biochemistry. Article e108755. https://doi.org/10.1016/j.plaphy.2024.108755.
DOI: https://doi.org/10.1016/j.plaphy.2024.108755

Interpretive Summary: As a model for understanding root defense processes in Beta vulgaris (sugarbeet), Glycine max (soybean) candidate defense genes have been identified that are expressed in a root cell undergoing a defense response to a pathogenic nematode, Heterodera glycines. It is hypothesized that the expression of the candidate soybean defense genes, polygalacturonase inhibiting proteins in a root of a soybean genotype that is normally not resistant to the pathogen will make it resistant to infection by H. glycines. Expressing one of these genes in a soybean genotype that is normally susceptible to H. glycines make the soybean resistant to pathogen attack. To determine if the gene type may function broadly among different crop plants, including sugar beet, cellular events that relate to the regulation of the expression of the candidate defense gene have been identified through artificial intelligence-mediated analyses.

Technical Abstract: Pathogen-secreted polygalacturonases (PGs) alter plant cell wall structure by cleaving the a3 (1'4) linkages between D-galacturonic acid residues in homogalacturonan (HG), macerating the cell wall, facilitating infection. Plant PG inhibiting proteins (PGIPs) disengage pathogen PGs, impairing infection. The soybean cyst nematode, Heterodera glycines, obligate root parasite produces secretions, generating a multinucleate nurse cell called a syncytium, a byproduct of the merged cytoplasm of 200-250 root cells, occurring through cell wall maceration. The common cytoplasmic pool, surrounded by an intact plasma membrane, provides a source from which H.glycines derives nourishment but without killing the parasitized cell during a susceptible reaction. The syncytium is also the site of a naturally-occurring defense response that happens in specific G. max genotypes. Transcriptomic analyses of RNA isolated from the syncytium undergoing the process of defense have identified that one of the 11 G. max PGIPs, GmPGIP11, is expressed during defense. Functional transgenic analyses show roots undergoing GmPGIP11 overexpression (OE) experience an increase in its relative transcript abundance (RTA) as compared to the ribosomal protein 21 (GmRPS21) control, leading to a decrease in H. glycines parasitism as compared to the overexpression control. The GmPGIP11 undergoing RNAi experiences a decrease in its RTA as compared to the GmRPS21 control with transgenic root experiencing an increase in H. glycines parasitism as compared to the RNAi control. Pathogen associated molecular pattern (PAMP) triggered immunity (PTI) and effector triggered immunity(ETI) components are shown to influence GmPGIP11 expression while numerous agricultural crops are shown to have homologs.