Differing Alterations of Two Esca Associated Fungi, Phaeoacremonium aleophilum and Phaeomoniella chlamydospora on Transcriptomic Level, to Co-Cultured Vitis vinifera L. calli

Abstract

The filamentous fungi Phaeoacremonium aleophilum (P.al, Teleomorph: Togninia minima) and Phaeomoniella chlamydospora (P.ch) are believed to be causal agents of wood symptoms associated with the Esca associated young vine decline. The occurrence of these diseases is dramatically increasing in vineyards all over the world whereas efficient therapeutic strategies are lacking. Both fungi occupy the same ecological niche within the grapevine trunk. We found them predominantly within the xylem vessels and surrounding cell walls which raises the question whether the transcriptional response towards plant cell secreted metabolites is comparable. In order to address this question we co-inoculated grapevine callus culture cells with the respective fungi and analyzed their transcriptomes by RNA sequencing. This experimental setup appears suitable since we aimed to investigate the effects caused by the plant thereby excluding all effects caused by other microorganisms omnipresent in planta and nutrient depletion. Bioinformatics analysis of the sequencing data revealed that 837 homologous genes were found to have comparable expression pattern whereas none of which was found to be differentially expressed in both strains upon exposure to the plant cells. Despite the fact that both fungi induced the transcription of oxido- reductases, likely to cope with reactive oxygen species produced by plant cells, the transcriptomics response of both fungi compared to each other is rather different in other domains. Within the transcriptome of P.ch beside increased transcript levels for oxido- reductases, plant cell wall degrading enzymes and detoxifying enzymes were found. On the other hand in P.al the transcription of some oxido- reductases was increased whereas others appeared to be repressed. In this fungus the confrontation to plant cells results in higher transcript levels of heat shock and chaperon-like proteins as well as genes encoding proteins involved in primary metabolism.

Xylem Vessel Diameter Affects the Compartmentalization of the Vascular Pathogen Phaeomoniella chlamydospora in Grapevine

“…Comparative genomic studies suggested that pectinolytic enzymatic activity for breaking-down pectin-rich compounds such as tyloses walls and gels play a central role in the fitness of vascular wilts ( Klosterman et al, 2011 ). Previous reports confirmed that P. chlamydospora could metabolize pectin while possessing a limited ability to break down cellulo-lignified secondary cell walls ( Surico et al, 2001 ; Santos et al, 2006 ; Valtaud et al, 2009 ; Fischer et al, 2016 ). Computational analysis of the P. chlamydospora genome also supported these conclusions ( Antonielli et al, 2014 ; Morales-Cruz et al, 2015 ).…”

Comparative pangenomic insights into the distinct evolution of virulence factors among grapevine trunk pathogens

“…Furthermore, apart from the extensive array of secondary metabolites in P. minimum, diverse virulence modes of action have been documented. These range from exopolysaccharides and polypeptides, causing varying degrees of disruption to water transport (10,84,85), to quinones and melanins, which shield the fungi against reactive oxygen species produced by plants as part of their defense mechanisms (10,(86)(87)(88). This suggests that changes in BGC gene content, and the corresponding secondary metabolites they produce, may be instrumental in adapting to new environmental conditions and could underlie a significant portion of intraspecific variations in virulence levels.…”

A Lipidomic Analysis of Leaves of Esca-Affected Grapevine Suggests a Role for Galactolipids in the Defense Response and Appearance of Foliar Symptoms

“…viticola challenge [ 7 , 9 ]. JA-mediated signaling has been associated with plant defense against necrotrophic pathogens and insects, inducing the accumulation of secondary metabolites and PR s; increased levels of phytoalexins and PR s is a common response of grapevine tissues to ESCA-associated fungi [ 5 , 33 , 35 , 45 ].…”

“…Plant response to pathogens is complex and composed of at least two layers: A basal, broad-band immunity called pathogen-associated molecular pattern-triggered immunity and a strain-specific level of immunity known as effector-triggered immunity. During the establishment of these immune responses, several compounds act as signals that trigger and mediate defense responses [ 5 , 6 , 7 , 8 , 9 ]. In general, the perception and communication of mechanisms triggered by each type of immunity are facilitated via Ca 2+ channels, mitogen-activated protein kinase (MAPK), nitric oxide (NO)-stimulated and reactive oxygen species (ROS)-regulated signaling cascades, which act as upstream sensors.…”

“…Esca complex disease (ESCA) is another GTD that attacks the perennial organs of grapevines, leading to tiger-stripe symptoms on leaves, apoplexy of shoots [ 2 , 3 ], and extensive wood necrosis (white rot, brown streaking, and other types of dark necrotic spots) on the trunk and cordons [ 26 ] colonized by fungi, such as Phaeomoniella chlamydospora [ 5 , 27 , 28 , 29 ], Phaeoacremonium minimum [ 5 , 30 ], Fomitiporia mediterranea [ 31 , 32 ], Botryosphaeriaceae species, and other fungal taxa [ 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 ]. Protection against GTDs relies mainly on prophylactic measures, remedial surgery [ 26 , 39 ], and the application of biological agents [ 8 , 31 ] or mixtures of fertilizers [ 40 , 41 ] to reduce symptom incidence and severity; these control strategies often offer only partial protection.…”