The Woody Plant-degrading Pathogen Lasiodiplodia Theobromae Effector LtCre1 Targets the Grapevine Sugar-signaling Protein VvRHIP1 to Suppress Host Immunity

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2023 Feb 15

PMID 36788641

Authors

Qikai Xing

Xiangui Zhou

Yang Cao

Junbo Peng

Wei Zhang

Xuncheng Wang

Jiahong Wu

Xinghong Li

Jiye Yan

Affiliations

Soon will be listed here.

Abstract

Lasiodiplodia theobromae is a causal agent of Botryosphaeria dieback, which seriously threatens grapevine production worldwide. Plant pathogens secrete diverse effectors to suppress host immune responses and promote the progression of infection, but the mechanisms underlying the manipulation of host immunity by L. theobromae effectors are poorly understood. In this study, we characterized LtCre1, which encodes a L. theobromae effector that suppresses BAX-triggered cell death in Nicotiana benthamiana. RNAi-silencing and overexpression of LtCre1 in L. theobromae showed impaired and increased virulence, respectively, and ectopic expression in N. benthamiana increased susceptibility. These results suggest that LtCre1 is as an essential virulence factor for L. theobromae. Protein-protein interaction studies revealed that LtCre1 interacts with grapevine RGS1-HXK1-interacting protein 1 (VvRHIP1). Ectopic overexpression of VvRHIP1 in N. benthamiana reduced infection, suggesting that VvRHIP1 enhances plant immunity against L. theobromae. LtCre1 was found to disrupt the formation of the VvRHIP1-VvRGS1 complex and to participate in regulating the plant sugar-signaling pathway. Thus, our results suggest that L. theobromae LtCre1 targets the grapevine VvRHIP1 protein to manipulate the sugar-signaling pathway by disrupting the association of the VvRHIP1-VvRGS1 complex.

Citing Articles

Advances in the molecular mechanism of grapevine resistance to fungal diseases.

Li Z, Wu R, Guo F, Wang Y, Nick P, Wang X Mol Hortic. 2025; 5(1):1.

PMID: 39743511 PMC: 11694456. DOI: 10.1186/s43897-024-00119-x.

References

Chethana K, Peng J, Li X, Xing Q, Liu M, Zhang W . LtEPG1, a Secretory Endopolygalacturonase Protein, Regulates the Virulence of in and Is Recognized as a Microbe-Associated Molecular Patterns. Phytopathology. 2020; 110(10):1727-1736. DOI: 10.1094/PHYTO-04-20-0118-R. View

Grigston J, Osuna D, Scheible W, Liu C, Stitt M, Jones A . D-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1. FEBS Lett. 2008; 582(25-26):3577-84. PMC: 2764299. DOI: 10.1016/j.febslet.2008.08.038. View

Dou D, Zhou J . Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe. 2012; 12(4):484-95. DOI: 10.1016/j.chom.2012.09.003. View

Wang J, Wang S, Hu K, Yang J, Xin X, Zhou W . The Kinase OsCPK4 Regulates a Buffering Mechanism That Fine-Tunes Innate Immunity. Plant Physiol. 2017; 176(2):1835-1849. PMC: 5813524. DOI: 10.1104/pp.17.01024. View

Zhang Y, Zhang K, Fang A, Han Y, Yang J, Xue M . Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nat Commun. 2014; 5:3849. DOI: 10.1038/ncomms4849. View

Dangl J, Horvath D, Staskawicz B . Pivoting the plant immune system from dissection to deployment. Science. 2013; 341(6147):746-51. PMC: 3869199. DOI: 10.1126/science.1236011. View

Cho Y, Yoo S, Sheen J . Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell. 2006; 127(3):579-89. DOI: 10.1016/j.cell.2006.09.028. View

Li Q, Ai G, Shen D, Zou F, Wang J, Bai T . A Phytophthora capsici Effector Targets ACD11 Binding Partners that Regulate ROS-Mediated Defense Response in Arabidopsis. Mol Plant. 2019; 12(4):565-581. DOI: 10.1016/j.molp.2019.01.018. View

Chen L, Hou B, Lalonde S, Takanaga H, Hartung M, Qu X . Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010; 468(7323):527-32. PMC: 3000469. DOI: 10.1038/nature09606. View

10.

Chen C, Liu S, Liu Q, Niu J, Liu P, Zhao J . An ANNEXIN-like protein from the cereal cyst nematode Heterodera avenae suppresses plant defense. PLoS One. 2015; 10(4):e0122256. PMC: 4388550. DOI: 10.1371/journal.pone.0122256. View

11.

Gramaje D, Urbez-Torres J, Sosnowski M . Managing Grapevine Trunk Diseases With Respect to Etiology and Epidemiology: Current Strategies and Future Prospects. Plant Dis. 2019; 102(1):12-39. DOI: 10.1094/PDIS-04-17-0512-FE. View

12.

Kretschmer M, Croll D, Kronstad J . Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation. Mol Plant Pathol. 2016; 18(9):1222-1237. PMC: 6638311. DOI: 10.1111/mpp.12486. View

13.

Sakr S, Wang M, Dedaldechamp F, Perez-Garcia M, Oge L, Hamama L . The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network. Int J Mol Sci. 2018; 19(9). PMC: 6165531. DOI: 10.3390/ijms19092506. View

14.

Boller T, He S . Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science. 2009; 324(5928):742-4. PMC: 2729760. DOI: 10.1126/science.1171647. View

15.

Fu Y, Lim S, Urano D, Tunc-Ozdemir M, Phan N, Elston T . Reciprocal encoding of signal intensity and duration in a glucose-sensing circuit. Cell. 2014; 156(5):1084-95. PMC: 4364031. DOI: 10.1016/j.cell.2014.01.013. View

16.

Yan J, Zhao W, Chen Z, Xing Q, Zhang W, Chethana K . Comparative genome and transcriptome analyses reveal adaptations to opportunistic infections in woody plant degrading pathogens of Botryosphaeriaceae. DNA Res. 2017; 25(1):87-102. PMC: 5824938. DOI: 10.1093/dnares/dsx040. View

17.

Yang T, Groenewald J, Cheewangkoon R, Jami F, Abdollahzadeh J, Lombard L . Families, genera, and species of Botryosphaeriales. Fungal Biol. 2017; 121(4):322-346. DOI: 10.1016/j.funbio.2016.11.001. View

18.

Jacobs K, Collins-Racie L, Colbert M, Duckett M, Kelleher K, Kriz R . A genetic selection for isolating cDNAs encoding secreted proteins. Gene. 1997; 198(1-2):289-96. DOI: 10.1016/s0378-1119(97)00330-2. View

19.

Boller T, Felix G . A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009; 60:379-406. DOI: 10.1146/annurev.arplant.57.032905.105346. View

20.

Cipriano A, Gondim D, Vasconcelos I, Martins J, Moura A, Moreno F . Proteomic analysis of responsive stem proteins of resistant and susceptible cashew plants after Lasiodiplodia theobromae infection. J Proteomics. 2014; 113:90-109. DOI: 10.1016/j.jprot.2014.09.022. View