The root-knot nematode (Meloidogyne incognita) produces a functional mimic of the Arabidopsis inflorescence deficient in abscission (IDA) signaling peptide

Authors: KIM, JOONYUP - University Of Maryland; Yang, Ronghui; CHANG, CAREN - University Of Maryland; Tucker, Mark

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/27/2018
Publication Date: 4/10/2018
Citation: Kim, J., Yang, R., Chang, C., Tucker, M.L. 2018. The root-knot nematode (Meloidogyne incognita) produces a functional mimic of the Arabidopsis inflorescence deficient in abscission (IDA) signaling peptide. Journal of Experimental Botany. 69(12):3009-3021. https://doi.org/10.1093/jxb/ery135.
DOI: https://doi.org/10.1093/jxb/ery135

Interpretive Summary: Nematodes, minute soil worms, are the most economically damaging pathogens of soybean. Pathogenic nematodes infect roots and induce the formation of a feeding structure, a specialized set of cells from which the nematodes acquire nutrients from the plant. The nematodes change the plant root cell biochemistry and physiology by co-opting developmental programs that are natural to the plant root. A plant protein named IDA has been demonstrated to be an important signal for the natural development of plant cells. We discovered and characterized an IDA-like gene and protein from a root-knot nematode. The IDA-like protein is similar to the plant IDA protein, but it alters cellular development in favor of the nematode. Inhibition of the IDA-like protein from the nematode reduced the nematode’s ability to infect plants. This research is leading to a new understanding of how nematodes induce the formation of a functional feeding structure in roots. These results are expected to be useful to scientists at universities, government agencies and companies who are trying to fight nematodes and the disease they cause on soybeans and other agriculturally important plants.

Technical Abstract: INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) is a signaling peptide that participates in the regulation of cell separation events in Arabidopsis including floral organ abscission and lateral root emergence. Sequence similarity searches (e.g., BLAST) of plant genomes have identified IDA-like (IDL) genes in all the dicotyledonous flowering plant genomes examined and a few monocots and gymnosperms. Of particular interest here, IDA-like genes were also found in the genomic sequences of root-knot nematodes, Meloidogyne sp, which are globally deleterious pathogens of agriculturally important plants, but the role of these genes are unknown. Exogenous treatment with synthetic peptide identical to the M. incognita IDA-like 1 (MiIDL1) protein sequence minus its N-terminal signal peptide recovered both the abscission and root architecture phenotypes of the Arabidopsis ida mutant. Moreover, constitutive expression of the full-length MiIDL1 open reading frame in Arabidopsis ida mutant plants substantially recovered the delayed floral organ abscission phenotype. By contrast, transformants containing a construct missing sequence for the MiIDL1 signal peptide retained the delayed abscission phenotype. In addition, wild-type Arabidopsis plants were transformed with inverted repeat (RNAi) constructs for the nematode MiIDL1 gene. At 35 and 42 days post nematode inoculation the MiIDL1 RNAi plants had approximately 40% fewer galls per root and smaller galls than the galls on control plants. These findings demonstrate that the nematode IDA-like gene, MiIDL1, produces a functional IDA mimic that can complement the Arabidopsis ida mutant phenotypes and reveal that MiIDL1 plays a significant role in the development of nematode galls on Arabidopsis roots.