Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao, interferes with cytokinin metabolism during infection of Micro-Tom tomato and promotes symptom development

被引:8
作者
Costa, Juliana L. [1 ]
Paschoal, Daniele [1 ,2 ]
da Silva, Eder M. [1 ]
Silva, Jamille S. [1 ,2 ]
do Carmo, Rafael M. [1 ]
Carrera, Esther [3 ]
Lopez-Diaz, Isabel [3 ]
Rossi, Monica L. [1 ]
Freschi, Luciano [4 ]
Mieczkowski, Piotr [5 ]
Peres, Lazaro E. P. [2 ]
Teixeira, Paulo J. P. L. [2 ,5 ]
Figueira, Antonio [1 ]
机构
[1] Univ Sao Paulo, Ctr Energia Nucl Agr, Ave Centenario 303, BR-13400970 Piracicaba, SP, Brazil
[2] Univ Sao Paulo, Escola Super Agr Luiz de Queiroz, Ave Padua Dias 9, BR-13418900 Piracicaba, SP, Brazil
[3] Univ Politecn Valencia UPV, CSIC, Inst Biol Mol & Celular Plantas, Ingeniero Fausto Elio S-N, Valencia 46022, Spain
[4] Univ Sao Paulo, Inst Biociencias, R Matao 321, BR-05508090 Sao Paulo, SP, Brazil
[5] Univ N Carolina, Chapel Hill, NC 27599 USA
基金
巴西圣保罗研究基金会;
关键词
cytokinin inhibitor; cytokinin oxidase; fruit locule number; hormonal imbalance; M82; Micro‐ Tom; tRNA‐ isopentenyl transferase; witches' broom disease; SALICYLIC-ACID; SOLANUM-LYCOPERSICON; THEOBROMA-CACAO; MODEL SYSTEM; GENE; SHOOT; INSIGHTS; HORMONES; PLANTS; AUXIN;
D O I
10.1111/nph.17386
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Moniliophthora perniciosa causes witches' broom disease of cacao and inflicts symptoms suggestive of hormonal imbalance. We investigated whether infection of the tomato (Solanum lycopersicum) model system Micro-Tom (MT) by the Solanaceae (S)-biotype of Moniliophthora perniciosa, which causes stem swelling and hypertrophic growth of axillary shoots, results from changes in host cytokinin metabolism. Inoculation of an MT-transgenic line that overexpresses the Arabidopsis CYTOKININ OXIDASE-2 gene (35S::AtCKX2) resulted in a reduction in disease incidence and stem diameter. RNA-sequencing analysis of infected MT and 35S::AtCKX2 revealed the activation of cytokinin-responsive marker genes when symptoms were conspicuous. The expression of an Moniliophthora perniciosa tRNA-ISOPENTENYL-TRANSFERASE suggests the production of isopentenyladenine (iP), detected in mycelia grown in vitro. Inoculated MT stems showed higher levels of dihydrozeatin and trans-zeatin but not iP. The application of benzyladenine induced symptoms similar to infection, whereas applying the cytokinin receptor inhibitors LGR-991 and PI55 decreased symptoms. Moniliophthora perniciosa produces iP that might contribute to cytokinin synthesis by the host, which results in vascular and cortex enlargement, axillary shoot outgrowth, reduction in root biomass and an increase in fruit locule number. This strategy may be associated with the manipulation of sink establishment to favour infection by the fungus.
引用
收藏
页码:365 / 381
页数:17
相关论文
共 80 条
[21]   CHARACTERIZATION OF AN ETHYLENE OVERPRODUCING MUTANT OF TOMATO (LYCOPERSICON-ESCULENTUM MILL CULTIVAR VFN8) [J].
FUJINO, DW ;
BURGER, DW ;
YANG, SF ;
BRADFORD, KJ .
PLANT PHYSIOLOGY, 1988, 88 (03) :774-779
[22]   Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem [J].
Gordon, Sean P. ;
Chickarmane, Vijay S. ;
Ohno, Carolyn ;
Meyerowitz, Elliot M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (38) :16529-16534
[23]   Manipulation of Phytohormone Pathways by Effectors of Filamentous Plant Pathogens [J].
Han, Xiaowei ;
Kahmann, Regine .
FRONTIERS IN PLANT SCIENCE, 2019, 10
[24]   Functional characterization of the first filamentous fungal tRNA-isopentenyltransferase and its role in the virulence of Claviceps purpurea [J].
Hinsch, Janine ;
Galuszka, Petr ;
Tudzynski, Paul .
NEW PHYTOLOGIST, 2016, 211 (03) :980-992
[25]   De novo biosynthesis of cytokinins in the biotrophic fungus Claviceps purpurea [J].
Hinsch, Janine ;
Vrabka, Josef ;
Oeser, Birgitt ;
Novak, Ondrej ;
Galuszka, Petr ;
Tudzynski, Paul .
ENVIRONMENTAL MICROBIOLOGY, 2015, 17 (08) :2935-2951
[26]   Distinct metabolism of N-glucosides of isopentenyladenine and trans-zeatin determines cytokinin metabolic spectrum in Arabidopsis [J].
Hosek, Petr ;
Hoyerova, Klara ;
Kiran, Nagavalli S. ;
Dobrev, Petre I. ;
Zahajska, Lenka ;
Filepova, Roberta ;
Motyka, Vaclav ;
Mueller, Karel ;
Kaminek, Miroslav .
NEW PHYTOLOGIST, 2020, 225 (06) :2423-2438
[27]  
Jefferson R A, 1987, EMBO J, V6, P3901
[28]   Linking development to defense: auxin in plant-pathogen interactions [J].
Kazan, Kemal ;
Manners, John M. .
TRENDS IN PLANT SCIENCE, 2009, 14 (07) :373-382
[29]   Side-Chain Modification of Cytokinins Controls Shoot Growth in Arabidopsis [J].
Kiba, Takatoshi ;
Takei, Kentaro ;
Kojima, Mikiko ;
Sakakibara, Hitoshi .
DEVELOPMENTAL CELL, 2013, 27 (04) :452-461
[30]   Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves [J].
Kilaru, Aruna ;
Bailey, Bryan A. ;
Hasenstein, Karl H. .
FEMS MICROBIOLOGY LETTERS, 2007, 274 (02) :238-244