Genome-wide characterisation and expression profile of the grapevine ATL ubiquitin ligase family reveal biotic and abiotic stress-responsive and development-related members

Abstract

The Arabidopsis Tóxicos en Levadura (ATL) protein family is a class of E3 ubiquitin ligases with a characteristic RING-H2 Zn-finger structure that mediates diverse physiological processes and stress responses in plants. We carried out a genome-wide survey of grapevine (Vitis vinifera L.) ATL genes and retrieved 96 sequences containing the canonical ATL RING-H2 domain. We analysed their genomic organisation, gene structure and evolution, protein domains and phylogenetic relationships. Clustering revealed several clades, as already reported in Arabidopsis thaliana and rice (Oryza sativa), with an expanded subgroup of grapevine-specific genes. Most of the grapevine ATL genes lacked introns and were scattered among the 19 chromosomes, with a high level of duplication retention. Expression profiling revealed that some ATL genes are expressed specifically during early or late development and may participate in the juvenile to mature plant transition, whereas others may play a role in pathogen and/or abiotic stress responses, making them key candidates for further functional analysis. Our data offer the first genome-wide overview and annotation of the grapevine ATL family, and provide a basis for investigating the roles of specific family members in grapevine physiology and stress responses, as well as potential biotechnological applications.

Co-expression network analysis and cis-regulatory element enrichment determine putative functions and regulatory mechanisms of grapevine ATL E3 ubiquitin ligases

“…Moreover, although BIN 29 (protein metabolism) was enriched in a total of 35 ATL subnetworks, none were common to all conditions. This indicates that, in accordance with the proposed sub-functionalization of ATL genes 20 , a given function may be carried out by different ATL genes depending on the conditions.

Figure 1 Number of grapevine ATL-centered co-expression clusters enriched in MapMan BIN categories under different conditions.

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“…The ATL family has been fully characterized in A . thaliana and rice 6 and was very recently identified in grapevine ( Vitis vinifera ), revealing 96 putative ATL genes 20 . At the functional level, only the EIRP1 protein from the wild species Vitis pseudoreticulata has been described thus far, in a report demonstrating its interaction with the defense-related transcription factor VpWRKY11 21 .…”

“…Gene regulation in response to physiological and developmental changes can be inferred from correlations among different co-expression networks. Grapevine ATL genes are expressed under diverse physiological conditions 20 , so we used multiple datasets representing abiotic and biotic stress as well as a condition-independent dataset. To unravel the regulatory mechanisms controlling ATL community clusters, we also identified cis -regulatory elements that are enriched in the promoters of the entire ATL gene family and in specific network modules.…”

Ubiquitin related enzymes and plant-specific ubiquitin ligase ATL family in tomato plants

“…A recent analysis of the ATL family in several plant species, including both monocot and eudicot species, was recently reported (Aguilar-Hernández et al 2011), as was a genome wide characterization of the ATL family in grapevine (Ariani et al 2016). Tomato is a major crop plant and a model system for fleshy fruit development (Shikata et al 2015;Tohge et al 2014).…”

CTLs, a new class of RING-H2 ubiquitin ligases uncovered by YEELL, a motif close to the RING domain that is present across eukaryotes

“…Indeed, the hydrophobic helix for some ATL proteins has been shown to be associated with the cell membranes [ 12 ]. An overview of the ATL family from grapevine and tomato have recently been reported [ 13 , 14 ]. BTL genes encode a different domain at the amino-terminus, that includes four cysteine residues resembling a C2/C2 Zinc Finger, known as BZF.…”