Alterations of plant architecture and phase transition by the phytoplasma virulence factor SAP11

Chang, Shu Heng; Tan, Choon Meng; Wu, Chih-Tang; Lin, Tzu-Hsiang; Jiang, Shin-Ying; Liu, Renci; Tsai, Mei-Ling; Su, Liwen; Yang, Jun-Yi

doi:10.1093/jxb/ery318

Cited by 56 publications

(102 citation statements)

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“…Although functional analyses of several effector homologs of phytoplasma have become areas of active research (Sugawara et al, 2013;Maejima et al, 2014;Chang et al, 2018;Wang et al, 2018b;Pecher et al, 2019), the evolutionary dynamics of these homologs…”

Section: Phyllogen Genes Can Be Horizontally Transferred Among Divementioning

confidence: 99%

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

Iwabuchi

Kitazawa

Maejima

et al. 2020

Molecular Plant Pathology

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Flower malformation represented by phyllody is a common symptom of phytoplasma infection induced by a novel family of phytoplasma effectors called phyllogens. Despite the accumulation of functional and structural phyllogen information, the molecular mechanisms of phyllody have not yet been integrated with their evolutionary aspects due to the limited data on their homologs across diverse phytoplasma lineages. Here, we developed a novel universal PCR‐based approach to identify 25 phytoplasma phyllogens related to nine “Candidatus Phytoplasma” species, including four species whose phyllogens have not yet been identified. Phylogenetic analyses showed that the phyllogen family consists of four groups (phyl‐A, ‐B, ‐C, and ‐D) and that the evolutionary relationships of phyllogens were significantly distinct from those of phytoplasmas, suggesting that phyllogens were transferred horizontally among phytoplasma strains and species. Although phyllogens belonging to the phyl‐A, ‐C, and ‐D groups induced phyllody, the phyl‐B group lacked the ability to induce phyllody. Comparative functional analyses of phyllogens revealed that a single amino acid polymorphism in phyl‐B group phyllogens prevented interactions between phyllogens and A‐ and E‐class MADS domain transcription factors (MTFs), resulting in the inability to degrade several MTFs and induce phyllody. Our finding of natural variation in the function of phytoplasma effectors provides new insights into molecular mechanisms underlying the aetiology of phytoplasma diseases.

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Section: Phyllogen Genes Can Be Horizontally Transferred Among Divementioning

confidence: 99%

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

Iwabuchi

Kitazawa

Maejima

et al. 2020

Molecular Plant Pathology

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“…In yeast, TE‐2‐6B, TE‐1‐6B‐L and TE‐1‐6B‐R were found to bind different subsets of TCP proteins. Differences in TCP‐binding patterns were also noted for some SAP11 variants (Chang et al , ; Wang et al , ). Strong Arabidopsis TCP phenotypes require simultaneous inactivation of several TCP genes (Efroni et al , ; Schommer et al , ; Koyama et al , ; Alvarez et al , ; Bresso et al , ).…”

Section: Discussionmentioning

confidence: 90%

“…Nicotiana benthamiana plants expressing SAP11 AYWB have wrinkled leaves (Tan et al , ) which resemble those of TE‐2‐6b N. tabacum plants (Chen et al , ). Although SAP11 AYWB localizes to the nucleus (Bai et al , ; Sugio et al , ), other SAP11‐like proteins are evenly distributed throughout the cell (Chang et al , ). Given the strong resemblance between the TE‐2‐6b , jaw‐D / TCP and SAP11 phenotypes, we hypothesized that TE‐2‐6b interferes with the miR319a/ TCP module.…”

Section: Introductionmentioning

confidence: 99%

Inhibition of Arabidopsis thaliana CIN‐like TCP transcription factors by Agrobacterium T‐DNA‐encoded 6B proteins

et al. 2019

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Summary Agrobacterium T‐DNA‐encoded 6B proteins cause remarkable growth effects in plants. Nicotiana otophora carries two cellular T‐DNAs with three slightly divergent 6b genes (TE‐1‐6b‐L, TE‐1‐6b‐R and TE‐2‐6b) originating from a natural transformation event. In Arabidopsis thaliana, expression of 2×35S:TE‐2‐6b, but not 2×35S:TE‐1‐6b‐L or 2×35S:TE‐1‐6b‐R, led to plants with crinkly leaves, which strongly resembled mutants of the miR319a/TCP module. This module is composed of MIR319A and five CIN‐like TCP (TEOSINTHE BRANCHED1, CYCLOIDEA and PROLIFERATING CELL NUCLEAR ANTIGEN BINDING FACTOR) genes (TCP2, TCP3, TCP4, TCP10 and TCP24) targeted by miR319a. The CIN‐like TCP genes encode transcription factors and are required for cell division arrest at leaf margins during development. MIR319A overexpression causes excessive growth and crinkly leaves. TE‐2‐6b plants did not show increased miR319a levels, but the mRNA levels of the TCP4 target gene LOX2 were decreased, as in jaw‐D plants. Co‐expression of green fluorescent protein (GFP)‐tagged TCPs with native or red fluorescent protein (RFP)‐tagged TE‐6B proteins led to an increase in TCP protein levels and formation of numerous cytoplasmic dots containing 6B and TCP proteins. Yeast double‐hybrid experiments confirmed 6B/TCP binding and showed that TE‐1‐6B‐L and TE‐1‐6B‐R bind a smaller set of TCP proteins than TE‐2‐6B. A single nucleotide mutation in TE‐1‐6B‐R enlarged its TCP‐binding repertoire to that of TE‐2‐6B and caused a crinkly phenotype in Arabidopsis. Deletion analysis showed that TE‐2‐6B targets the TCP4 DNA‐binding domain and directly interferes with transcriptional activation. Taken together, these results provide detailed insights into the mechanism of action of the N. otophora TE‐encoded 6b genes.

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“…SAP54 mediates degradation of MIKC MADS-box transcription factors involved in floral development and induces phyllody (MacLean et al, 2014). SAP11 binds and destabilizes certain TCP transcription factors involved in axillary meristem outgrowth, leaf shape determination and jasmonate signalling, leading to an altered morphology and decreased plant defense (Sugio et al, 2011b;Chang et al, 2018;Wang et al, 2018). Finally, TENGU causes dwarfism, witches' broom and arrested flower development.…”

Section: Introductionmentioning

confidence: 99%

Protein interaction mapping reveals widespread targeting of development-related host transcription factors by phytoplasma effectors

Marrero

Capdevielle

Huang

et al. 2020

Preprint

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This work shows that the effectors of phytoplasma, a bacterial plant pathogen, show pervasive interactions with development-related host transcription factors, providing a way to take over plant growth and development in favor of the pathogen and its insect vector. The obtained comprehensive protein interaction network and showcase of the potential biological consequences of a selected effector advance our understanding of phytoplasma-host interactions and provide guidance for further study.

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Alterations of plant architecture and phase transition by the phytoplasma virulence factor SAP11

Abstract: Phytoplasma SAP11 effectors acquired fundamental activity in destabilizing TB/CYC-TCPs, the key factors controlling axillary meristem development, and serve as core virulence factors responsible for the witches’ broom symptom.

Cited by 56 publications

References 56 publications

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

Inhibition of Arabidopsis thaliana CIN‐like TCP transcription factors by Agrobacterium T‐DNA‐encoded 6B proteins

Protein interaction mapping reveals widespread targeting of development-related host transcription factors by phytoplasma effectors

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