Soybean GmSAUL1, a bona fide U-Box E3 ligase, negatively regulates immunity likely through repressing the activation of GmMPK3

Authors: LI, JUN-MEI - Zhejiang Normal University; YE, MEI-YAN - Zhejiang Normal University; WANG, CHAOFENG - University Of Nebraska; MA, XIAO-HAN - Zhejiang Normal University; WU, NI-NI - Zhejiang Normal University; ZOHNG, CHEN-LI - Zhejiang Normal University; ZHANG, YANJUN - Zhejiang Normal University; CHENG, NINGHUI - Children'S Nutrition Research Center (CNRC); Nakata, Paul; ZENG, LIRONG - University Of Nebraska; LIU, JIAN-ZHONG - Zhejiang Normal University

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/14/2023
Publication Date: 3/25/2023
Citation: Li, J., Ye, M., Wang, C., Ma, X., Wu, N., Zohng, C., Zhang, Y., Cheng, N., Nakata, P.A., Zeng, L., Liu, J. 2023. Soybean GmSAUL1, a bona fide U-Box E3 ligase, negatively regulates immunity likely through repressing the activation of GmMPK3. International Journal of Molecular Sciences. 24. Article 6240. https://doi.org/10.3390/ijms24076240.
DOI: https://doi.org/10.3390/ijms24076240

Interpretive Summary: Plant pathogens often infect crop plants resulting in reduced yields, quality, and profitability. Thus, scientists have been avidly searching for ways to increase the plant's immunity to these pathogens. In this study we investigate the role of a gene called SAUL1 in plant immunity. Gene silencing studies revealed that a reduction in SAUL1 expression in soybean resulted in an activation of plant defense genes suggesting that SAUL1 played a negative role in plant immunity. Over-expression of SAUL1 in tobacco; however, resulted in a similar increase in plant defense genes suggesting that SAUL1 played a positive role in plant immunity in this plant. Taken together, it appears SAUL1 could play both a positive and negative role in regulating plant immunity in certain circumstances. It is our hope that by studying this complex process of plant immunity we will gain a level of understanding that will allow us to eventually design strategies to combat plant pathogens and improve the yields, quality, and profitability of crop plants.

Technical Abstract: E3 Ubiquitin Ligases play important roles in plant immunity. Although well studied in Arabidopsis, the role of E3 ubiquitin ligases in immunity has not been extensively investigated in soybean. In this report, we used Bean pod mottle virus (BPMV)-mediated virus-induced gene silencing (VIGS) to investigate the function of GmSAUL1 (Senescence-Associated E3 Ubiquitin Ligase 1) homologs in soybean defense responses. When two closely related SAUL1, referred to as GmSAUL1a and GmSAUL1b, respectively, were silenced simultaneously, the soybean plants displayed autoimmune phenotypes including stunted statures, spontaneous cell death, significantly elevated level of both reactive oxygen species (ROS) and salicylic acid (SA), increased expression of the PR genes and enhanced resistance to viral and bacterial pathogens. These results indicated that GmSAUL1a/1b play a negative role in immune response in soybean. The activated immune responses observed in the GmSAUL1a/1b-silenced plants were significantly alleviated by co-silencing GmICS1a/1b or GmEDS1a/1b as well as by high temperature treatment, suggesting that GmSAUL1a/1b might be guarded by an R protein that depends on the SA pathway. Unexpectedly, we found that ectopic over-expression of GmSAUL1a in N. tobacum similarly resulted in autoimmunity that could be suppressed by high temperature, indicating that the GmSAUL1a plays a positive regulatory role in immunity that depends upon the activation of the R protein(s). Interestingly, whereas silencing GmSAUL1a/1b resulted in a decreased activation of GmMPK6 and an increased activation of GmMPK3 in response to flg22 treatment, ectopic over-expression of the GmSAUL1a in N. tobacum led to an elevated activation of NtMPK6 but reduced activation of NtMPK4 upon flg22 elicitation, suggesting that silencing GmSAUL1a/1b and over-expressing GmSAUL1a activated immune signaling through different downstream MAPK signaling modules. Furthermore, we provided evidence that GmSAUL1a was a bona fide E3 ligase. Collectively, our results indicated that GmSAUL1 plays both positive and negative roles in regulating cell death and immunity.