Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism

Authors: RAMBANI, ADITI - University Of Tennessee; PANTALONE, VINCE - University Of Tennessee; YANG, SONGNAN - University Of Tennessee; RICE, HOLLIS - University Of Tennessee; Song, Qijian; MAZAREI, MITRA - University Of Tennessee; Arelli, Prakash; MEKSEM, KHALID - Southern Illinois University; STEWART, NEAL - University Of Tennessee; HEWEZI, TAREK - University Of Tennessee

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/18/2020
Publication Date: 2/28/2020
Citation: Rambani, A., Pantalone, V., Yang, S., Rice, H., Song, Q., Mazarei, M., Arelli, P.R., Meksem, K., Stewart, N., Hewezi, T. 2020. Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. New Phytologist. 227(1):168-184. https://doi.org/10.1111/nph.16511.
DOI: https://doi.org/10.1111/nph.16511

Interpretive Summary: Soybean cyst nematode (SCN) is the most damaging soybean pathogen, causing significant yield and quality losses. Resistance to SCN is conferred by two main soybean DNA regions, Rhg1 and Rhg4, at chromosome 18 and 8, respectively. The Rhg1 region contains three genes within a repeat region. Increased expression of these three genes contributes to SCN resistance in an additive manner. The Rhg4 locus contains only one gene encoding serine hydroxymethyltransferase (GmSHMT08). Most SCN resistant soybeans contain Rhg1 or both the Rhg4 and Rhg1. Soybeans only having Rhg1 display slow degeneration of the nematode feeding site, leading to delayed arrest of nematode development. Soybeans with both Rhg4 and Rhg1 have stronger and faster resistance, leading to rapid arrest of nematode development during the infective juvenile stage. The molecular mechanisms through which Rhg4 mediates SCN resistance remain to be elucidated. In this study, the function of GmSHMT08 in establishing DNA methylation landscapes of soybean roots during SCN infection was studied using highly homozygous near-isogenic soybean differing at Rhg4. We observed that the susceptible soybean exhibited reduced DNA methylation levels in both protein-coding genes and transposable elements, whereas the resistant line showed the opposite response in response to SCN infection. This trend was observed in all DNA methylation contexts, suggesting that GmSHMT08's function is vital for cellular methyltransferase activity. Our analyses provide unprecedented insights into the biochemical basis of GmSHMT08 function in SCN resistance and provide insights into the role of GmSHMT08 in regulating soybean DNA through methylation. Scientists at universities, government agencies, and private institutes will be able to use this knowledge to to help shape soybean defense responses upon SCN infection.

Technical Abstract: Rhg4 is a major locus required for soybean cyst nematode (SCN) resistance in certain soybean accessions. Rhg4 encodes a serine hydroxymethyltransferase (GmSHMT08), whose function in nematode resistance remains mostly unknown. In this study, we revealed a key role of GmSHMT08 in reprograming the soybean methylome during SCN infection using a pair of highly homozygous near-isogenic lines (NILs) differing at GmSHMT08. Under non-infected conditions, the genomes of the NILs were considerably differentially methylated, and this difference was associated with differential gene expression that may prime their responses to SCN parasitism. In response to SCN infection, the susceptible line exhibited reduced global methylation levels in both protein-coding genes and transposable elements, whereas the resistant line showed the opposite response of increased global methylation levels. This trend was observed in all DNA methylation contexts, suggesting that GmSHMT08's function is vital for cellular methyltransferase activity. Comparing the methylomes of the parental lines with that of the NILs resulted in the identification of heritable and novel non-parental differentially methylated regions overlapping with genes associated with soybean response to SCN infection. Altogether, our analyses provide unprecedented insights into the role of GmSHMT08 in reprograming the soybean methylome that may shape plant response upon SCN infection.