Apoplastic and intracellular plant sugars regulate developmental transitions in witches’ broom disease of cacao

Barau, Joan; Grandis, Adriana; Carvalho, Vinicius Miessler de Andrade; Teixeira, Gleidson Silva; Zaparoli, G.; Rio, Maria Carolina Scatolin do; Rincones, Johana; Buckeridge, Marcos Silveira; Pereira, Gonçalo Amarante Guimarães

doi:10.1093/jxb/eru485

Cited by 24 publications

(38 citation statements)

References 77 publications

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“…These sugars have been detected in tissues of arabidopsis infected with the virulent D188 strain . As sugars have recently been identified as key components of the release of apical dominance (Barbier et al, 2015), a high sugar environment may be the signal for multiple bud formation, as suggested for witches' broom disease of cacao (Barau et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Dhandapani

Song

Novák

et al. 2016

Ann Bot

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Background and Aims Pisum sativum L. (pea) seed is a source of carbohydrate and protein for the developing plant. By studying pea seeds inoculated by the cytokinin-producing bacterium, Rhodococcus fascians, we sought to determine the impact of both an epiphytic (avirulent) strain and a pathogenic strain on source-sink activity within the cotyledons during and following germination.Methods Bacterial spread was monitored microscopically, and real-time reverse transcription-quantitative PCR was used to determine the expression of cytokinin biosynthesis, degradation and response regulator gene family members, along with expression of family members of SWEET, SUT, CWINV and AAP genes -gene families identified initially in pea by transcriptomic analysis. The endogenous cytokinin content was also determined.Key Results The cotyledons infected by the virulent strain remained intact and turned green, while multiple shoots were formed and root growth was reduced. The epiphytic strain had no such marked impact. Isopentenyl adenine was elevated in the cotyledons infected by the virulent strain. Strong expression of RfIPT, RfLOG and RfCKX was detected in the cotyledons infected by the virulent strain throughout the experiment, with elevated expression also observed for PsSWEET, PsSUT and PsINV gene family members. The epiphytic strain had some impact on the expression of these genes, especially at the later stages of reserve mobilization from the cotyledons.Conclusions The pathogenic strain retained the cotyledons as a sink tissue for the pathogen rather than the cotyledon converting completely to a source tissue for the germinating plant. We suggest that the interaction of cytokinins, CWINVs and SWEETs may lead to the loss of apical dominance and the appearance of multiple shoots.

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Section: Discussionmentioning

confidence: 99%

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Dhandapani

Song

Novák

et al. 2016

Ann Bot

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“…These chlorotic and swollen shoots are formed as a consequence of a hormonal imbalance and intense reprogramming of the plant metabolism induced by the fungal infection (4,5). The necrotrophic phase of the disease begins upon death of plant tissues, which are invaded by the proliferative mycelia.…”

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confidence: 99%

Plant pathogenesis–related proteins of the cacao fungal pathogen Moniliophthora perniciosa differ in their lipid-binding specificities

Darwiche

Atab

Baroni

et al. 2017

Journal of Biological Chemistry

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“…A infecção de flores em desenvolvimento promove a formação de frutos paternocárpicos e reversão de almofadas florais em ramos vegetativos, enquanto que a colonização de frutos em desenvolvimento leva à podridão dos mesmos (Purdy & Schmidt, 1996) (Figura 1). A fase biotrófica prolongada de infecção e os sintomas característicos da doença sugerem que este patógeno induza e/ou manipule o metabolismo primário e o balanço hormonal de sua planta hospedeira (Scarpari et al, 2005;Teixeira et al, 2014;Barau et al, 2014).…”

Section: A Interação M Perniciosa X T Cacaounclassified

“…A avaliação de carboidratos especificamente no apoplasto de vassouras-verdes de cacaueiro demonstrou a alteração dinâmica de açúcares após a infecção por M. perniciosa (Barau et al, 2014). Altos níveis de glicose e frutose contrastaram os níveis reduzidos de sacarose, tendo em vista a atividade da enzima invertase.…”

Section: Alterações Bioquímicas Decorrentes Da Infecção Por M Pernicunclassified

“…O estudo da patogenicidade de M. perniciosa é bastante relevante devido ao extenso período biotrófico de infecção por esse patógeno, por meio da colonização do apoplasto, por micélio desprovido de estruturas especializadas para nutrição (Teixeira et al, 2014). A despeito da colonização em baixas densidades dos tecidos infectados (Penman et al, 2000;Sena et al, 2014), a infecção pelos biótipos -C e -S de M. perniciosa promove a formação de sintomas notáveis, com alterações morfológicas, hormonais, fisiológicas e bioquímicas marcantes em cacaueiro (Purdy & Schmidt, 1996;Scarpari et al, 2005;Teixeira et al, 2014;Barau et al, 2014) e em MT (Costa, 2017), respectivamente.…”

Section: Introductionunclassified

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Análise metabolômica da interação Moniliophthora perniciosa x Solanum lycopersicum

Paschoal¹

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Witches' broom is a major disease of cacao, limiting cocoa production in South America. The basidiomycete Moniliophthora perniciosa, the disease causative agent, presents hemibiotrophic lifestyle with an extensive biotrophic period, promoting typical symptoms of hypertrophic growth of stems and proliferation of axillary shoots. The tomato (Solanum lycopersicum) cv. 'Micro-Tom' (MT) is a suitable genetic model to study pathogenic interaction of S-biotype M. perniciosa, exhibiting typical symptoms of the infection. Considering the lack of knowledge regarding biochemical and physiological mechanisms of M. perniciosa pathogenesis, this study aimed to investigate physiological and metabolic changes during MT infection of M. perniciosa. Inoculation of M. perniciosa caused stem thickening, leaf chlorosis and reduction in root growth and fruits in MT. We also observed a decline in photosynthetic rate (A), stomatal closure, increase in intracellular CO2, decrease in leaf transpiration and an increase on stem Proline, polyamines, and ascorbate oxidation exhibits an oxidative stress environment at the site of MT infection, whereas the accumulation of raffinose and GABA suggests ROS neutralization, mitigating its harmful effects. At 30 DAI, carbon reallocation and sugar signaling pathways were shifted. Sucrose exogenous application in MT infected plants by M. perniciosa reduced symptoms of stem swelling, but did not reduce root growth or number of fruits. Inoculation of single-flower truss sft mutant and its opposite 35S::SFT with M. pernciosa demonstrated that pathogen infection did not affect transition from vegetative to reproductive meristem, but decreased the development of flowers. Finally, inoculation of lutescent and green flesh senescence mutants neither altered symptoms of infection, nor enabled the observation of necrosis of infected tissue in MT background, as observed in cacao infected by M. perniciosa. A model for biochemical and physiological changes during MT infection by M. perniciosa was proposed.

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Apoplastic and intracellular plant sugars regulate developmental transitions in witches’ broom disease of cacao

Abstract: HighlightPhytopathogens can co-opt plant primary metabolism to enhance pathogenesis and pathogen nutrition. In witches’ broom disease of cacao, sensing and modulation of compartmentalized carbon availability can also temporally regulate disease development.

Cited by 24 publications

References 77 publications

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Plant pathogenesis–related proteins of the cacao fungal pathogen Moniliophthora perniciosa differ in their lipid-binding specificities

Análise metabolômica da interação Moniliophthora perniciosa x Solanum lycopersicum

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