Is  Zymoseptoria tritici  a hemibiotroph?

Sánchez‐Vallet, Andrea; McDonald, Megan C.; Solomon, Peter S.; McDonald, Bruce A.

doi:10.1016/j.fgb.2015.04.001

Cited by 86 publications

(83 citation statements)

References 53 publications

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“…An alternative explanation is that these proteins play a defensive role by inactivating pathogenesis‐related (PR) proteins, which are part of the plant's basal defences (Edreva, ). The use of pathogen proteases to inactivate host basal defences would fit the model of latent necrotrophy recently proposed for Z. tritici (Sanchez‐Vallet et al ., ). This model is also supported by the fact that none of the other groups of secreted hydrolytic enzymes considered in our analyses are highly expressed during the biotrophic phase, suggesting that nutrient acquisition is not very active during the asymptomatic phase.…”

Section: Resultsmentioning

confidence: 97%

Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles

Palma‐Guerrero

Torriani

Zala

et al. 2016

Molecular Plant Pathology

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Zymoseptoria tritici causes Septoria tritici blotch (STB) on wheat. The disease interaction is characterized by clearly defined temporal phases of infection, ultimately resulting in the death of host tissue. Zymoseptoria tritici is a highly polymorphic species with significant intraspecific variation in virulence profiles. We generated a deep transcriptomic sequencing dataset spanning the entire time course of an infection using a previously uncharacterized, highly virulent Z. tritici strain isolated from a Swiss wheat field. We found that seven clusters of gene transcription profiles explained the progression of the infection. The earliest highly up-regulated genes included chloroperoxidases, which may help the fungus cope with plant defences. The onset of necrotrophy was characterized by a concerted up-regulation of proteases, plant cell wall-degrading enzymes and lipases. Functions related to nutrition and growth characterized late necrotrophy and the transition to saprotrophic growth on dead plant tissue. We found that the peak up-regulation of genes essential for mating coincided with the necrotrophic phase. We performed an intraspecies comparative transcriptomics analysis using a comparable time course infection experiment of the genome reference isolate IPO323. Major components of the fungal infection transcriptome were conserved between the two strains. However, individual small, secreted proteins, proteases and cell wall-degrading enzymes showed strongly differentiated transcriptional profiles between isolates. Our analyses illustrate that successful STB infections involve complex transcriptomic remodelling to up-regulate distinct gene functions. Heterogeneity in transcriptomes among isolates may explain some of the considerable variation in virulence and host specialization found within the species.

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Section: Resultsmentioning

confidence: 97%

Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles

Palma‐Guerrero

Torriani

Zala

et al. 2016

Molecular Plant Pathology

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“…While necrotrophic feeding is essential for the completion of the Z. tritici life cycle, the lack of haustorial development for nutrient acquisition seems to point away from the hallmarks of a biotrophic pathogen and towards that of an endophyte (Goodwin et al , ; Sánchez‐Vallet et al , ). An absence of dedicated feeding structures, a non‐injurious method of entry, non‐invasive occupation of the apoplast during the latent phase, a reduced suite of genes encoding putative cell wall‐degrading enzymes (CWDEs) and the partial completion of the life cycle within a host are all attributes of Z. tritici .…”

Section: The Known Unknownsmentioning

confidence: 99%

“…There may, of course, have been minute increases in biomass that were not discernible by the qPCR methods used to detect Z. tritici in planta (Shetty et al , ). Hence, the term ‘latent necrotroph’ as opposed to ‘hemibiotroph’ was proposed as a more fitting definition for Z. tritici (Sánchez‐Vallet et al , ). Either the fungus is surviving on subsistence feeding during the initial phase of infection or quite possibly, as proposed by Keon et al (), the fungus is using its own energy reserves during the initial stages of infection and enters a state of starvation.…”

Section: The Known Unknownsmentioning

confidence: 99%

A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

et al. 2019

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Septoria tritici blotch (STB) disease of wheat is caused by the fungal pathogen Zymoseptoria tritici. It is the most important foliar disease of wheat in western Europe and affects wheat cultivation worldwide. The combination of intensive fungicide usage, a polycyclic asexual life cycle and an active sexual cycle has led to the emergence of fungal strains resistant/tolerant to all the major classes of fungicides used in its control. The hallmark of this disease is a long, symptomless latent phase that precedes the onset of visible symptoms. Understanding the processes that occur during the symptomless phase of infection is paramount in developing alternative strategies for disease control; however, large gaps in our knowledge of the disease remain. The known unknowns of the latent stage of infection can be summarized in three questions. Does the fungus initiate or manipulate host defences to trigger programmed cell death in order to facilitate nutrient acquisition or is the host acting exclusively? Does the fungus feed during both the latent phase and the necrotrophic phase like a true hemibiotroph? Does the long latent phase serve a beneficial function for the fungus or is it simply an artefact of evolution? This review aims to distil observations made during studies that have directly or indirectly contributed to answering these questions and points towards their most likely answers.

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“…It is an apoplastic pathogen with a latent necrotrophic lifestyle (Sánchez‐Vallet et al ., 2015). Fungal hyphae penetrate the stomata and colonise the apoplast during a long asymptomatic phase that lasts between 7 and 14 d, depending on the weather conditions, the host cultivar and the pathogen strain.…”

Section: Introductionmentioning

confidence: 99%

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

et al. 2018

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Summary Cultivar‐strain specificity in the wheat–Zymoseptoria tritici pathosystem determines the infection outcome and is controlled by resistance genes on the host side, many of which have been identified. On the pathogen side, however, the molecular determinants of specificity remain largely unknown.We used genetic mapping, targeted gene disruption and allele swapping to characterise the recognition of the new avirulence factor Avr3D1. We then combined population genetic and comparative genomic analyses to characterise the evolutionary trajectory of Avr3D1.Avr3D1 is specifically recognised by wheat cultivars harbouring the Stb7 resistance gene, triggering a strong defence response without preventing pathogen infection and reproduction. Avr3D1 resides in a cluster of putative effector genes located in a genome region populated by independent transposable element insertions. The gene was present in all 132 investigated strains and is highly polymorphic, with 30 different protein variants identified. We demonstrated that specific amino acid substitutions in Avr3D1 led to evasion of recognition.These results demonstrate that quantitative resistance and gene‐for‐gene interactions are not mutually exclusive. Localising avirulence genes in highly plastic genomic regions probably facilitates accelerated evolution that enables escape from recognition by resistance proteins.

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Is Zymoseptoria tritici a hemibiotroph?

Cited by 86 publications

References 53 publications

Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles

Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles

A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

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