The Alteration of Plant Morphology by Small Peptides Released from the Proteolytic Processing of the Bacterial Peptide TENGU

Overview

Journal Plant Physiol

Specialty Physiology

Date 2013 Jun 21

PMID 23784461

Citations 28

Authors

Kyoko Sugawara

Youhei Honma

Ken Komatsu

Misako Himeno

Kenro Oshima

Shigetou Namba

Affiliations

Soon will be listed here.

Abstract

Phytoplasmas are insect-borne plant pathogenic bacteria that alter host morphology. TENGU, a small peptide of 38 residues, is a virulence factor secreted by phytoplasmas that induces dwarfism and witches' broom in the host plant. In this study, we demonstrate that plants process TENGU in order to generate small functional peptides. First, virus vector-mediated transient expression demonstrated that the amino-terminal 11 amino acids of TENGU are capable of causing symptom development in Nicotiana benthamiana plants. The deletion of the 11th residue significantly diminished the symptom-inducing activity of TENGU, suggesting that these 11 amino acids constitute a functional domain. Second, we found that TENGU undergoes proteolytic processing in vitro, generating peptides of 19 and 21 residues including the functional domain. Third, we observed similar processing of TENGU in planta, and an alanine substitution mutant of TENGU, for which processing was compromised, showed reduced symptom induction activity. All TENGU homologs from several phytoplasma strains possessed similar symptom induction activity and went through processing, which suggests that the processing of TENGU might be related to its function.

Citing Articles

The crotonylated and succinylated proteins of jujube involved in phytoplasma-stress responses.

Zhang L, Wang H, Xue C, Liu Y, Zhang Y, Liu Z BMC Biol. 2024; 22(1):113.

PMID: 38750524 PMC: 11094900. DOI: 10.1186/s12915-024-01917-x.

Phytoplasma: A plant pathogen that cannot be ignored in agricultural production-Research progress and outlook.

Wang R, Bai B, Li D, Wang J, Huang W, Wu Y Mol Plant Pathol. 2024; 25(2):e13437.

PMID: 38393681 PMC: 10887288. DOI: 10.1111/mpp.13437.

PhyEffector, the First Algorithm That Identifies Classical and Non-Classical Effectors in Phytoplasmas.

Carreon-Anguiano K, Vila-Luna S, Saenz-Carbonell L, Canto-Canche B Biomimetics (Basel). 2023; 8(7).

PMID: 37999191 PMC: 10669590. DOI: 10.3390/biomimetics8070550.

Potential mobile units drive the horizontal transfer of phytoplasma effector genes.

Tokuda R, Iwabuchi N, Kitazawa Y, Nijo T, Suzuki M, Maejima K Front Genet. 2023; 14:1132432.

PMID: 37252660 PMC: 10210161. DOI: 10.3389/fgene.2023.1132432.

The genome of Candidatus phytoplasma ziziphi provides insights into their biological characteristics.

Xue C, Zhang Y, Li H, Liu Z, Gao W, Liu M BMC Plant Biol. 2023; 23(1):251.

PMID: 37173622 PMC: 10176825. DOI: 10.1186/s12870-023-04243-6.

References

Kakizawa S, Oshima K, Ishii Y, Hoshi A, Maejima K, Jung H . Cloning of immunodominant membrane protein genes of phytoplasmas and their in planta expression. FEMS Microbiol Lett. 2009; 293(1):92-101. DOI: 10.1111/j.1574-6968.2009.01509.x. View

Khang C, Berruyer R, Giraldo M, Kankanala P, Park S, Czymmek K . Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell. 2010; 22(4):1388-403. PMC: 2879738. DOI: 10.1105/tpc.109.069666. View

Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K, Migdoll A . The linear chromosome of the plant-pathogenic mycoplasma 'Candidatus Phytoplasma mali'. BMC Genomics. 2008; 9:306. PMC: 2459194. DOI: 10.1186/1471-2164-9-306. View

Guo Y, Ni J, Denver R, Wang X, Clark S . Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis. Plant Physiol. 2011; 157(1):476-84. PMC: 3165893. DOI: 10.1104/pp.111.180554. View

Christensen N, Axelsen K, Nicolaisen M, Schulz A . Phytoplasmas and their interactions with hosts. Trends Plant Sci. 2005; 10(11):526-35. DOI: 10.1016/j.tplants.2005.09.008. View

Matsubayashi Y, Sakagami Y . Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci U S A. 1996; 93(15):7623-7. PMC: 38796. DOI: 10.1073/pnas.93.15.7623. View

Srivastava R, Liu J, Howell S . Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J. 2008; 56(2):219-227. PMC: 2667306. DOI: 10.1111/j.1365-313X.2008.03598.x. View

Fletcher J, Brand U, Running M, Simon R, Meyerowitz E . Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 1999; 283(5409):1911-4. DOI: 10.1126/science.283.5409.1911. View

Tran-Nguyen L, Kube M, Schneider B, Reinhardt R, Gibb K . Comparative genome analysis of "Candidatus Phytoplasma australiense" (subgroup tuf-Australia I; rp-A) and "Ca. Phytoplasma asteris" Strains OY-M and AY-WB. J Bacteriol. 2008; 190(11):3979-91. PMC: 2395047. DOI: 10.1128/JB.01301-07. View

10.

Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimoto M . A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol. 2011; 85(19):10269-78. PMC: 3196401. DOI: 10.1128/JVI.05273-11. View

11.

Hoshi A, Oshima K, Kakizawa S, Ishii Y, Ozeki J, Hashimoto M . A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proc Natl Acad Sci U S A. 2009; 106(15):6416-21. PMC: 2669400. DOI: 10.1073/pnas.0813038106. View

12.

Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y . Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science. 2010; 329(5995):1065-7. DOI: 10.1126/science.1191132. View

13.

Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H . A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science. 2006; 313(5788):845-8. DOI: 10.1126/science.1128439. View

14.

Kakizawa S, Oshima K, Jung H, Suzuki S, Nishigawa H, Arashida R . Positive selection acting on a surface membrane protein of the plant-pathogenic phytoplasmas. J Bacteriol. 2006; 188(9):3424-8. PMC: 1447460. DOI: 10.1128/JB.188.9.3424-3428.2006. View

15.

Rafiqi M, Gan P, Ravensdale M, Lawrence G, Ellis J, Jones D . Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell. 2010; 22(6):2017-32. PMC: 2910983. DOI: 10.1105/tpc.109.072983. View

16.

Oshima K, Shiomi T, Kuboyama T, Sawayanagi T, Nishigawa H, Kakizawa S . Isolation and Characterization of Derivative Lines of the Onion Yellows Phytoplasma that Do Not Cause Stunting or Phloem Hyperplasia. Phytopathology. 2008; 91(11):1024-9. DOI: 10.1094/PHYTO.2001.91.11.1024. View

17.

Wang X, Mitchum M, Gao B, Li C, Diab H, Baum T . A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol. 2010; 6(2):187-91. DOI: 10.1111/j.1364-3703.2005.00270.x. View

18.

Reid D, Ferguson B, Gresshoff P . Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact. 2011; 24(5):606-18. DOI: 10.1094/MPMI-09-10-0207. View

19.

Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M . Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci U S A. 2008; 105(39):15208-13. PMC: 2567516. DOI: 10.1073/pnas.0808444105. View

20.

Clark S . Cell signalling at the shoot meristem. Nat Rev Mol Cell Biol. 2001; 2(4):276-84. DOI: 10.1038/35067079. View