having high homology with Arabidopsis NAC proteins associated with stress responses
such as SOG1 (SUPPRESSOR OF GAMMA RESPONSE 1) (Yoshiyama 2016) and
with vascular development such as SND2 (SECONDARY WALL-ASSOCIATED
NAC DOMAIN PROTEIN 2) and SND3 involved in secondary cell wall formation.
The identification of NAC TFs in this group of green algae could suggest an essential
role for NAC proteins in protecting the cell against the stresses associated with the
adaptation of plants to a terrestrial environment (Maugarny-Calès et al. 2016).
If the number of NAC genes present in different species is compared throughout
evolution, an expansion of the NAC TF family is observed after the divergence of
tracheophytes. This expansion appears to have arisen through gene duplication or
whole-genome duplication, creating paralogous genes with a high degree of sequence
similarity and functional redundancy (Singh et al. 2013; Wang et al. 2013b). Recent
studies suggest that both tandem and segmental duplication might have played a key role
in the expansion of the NAC family (Puranik et al. 2013; Singh et al. 2013; Wang et al.
2013b; You et al. 2015). In E. grandis, more than 60% of the NAC genes are distributed in tandem in their genome, while in S. tuberosum, V. vinifera and P. trichocarpa,
such expansion has occurred mainly by segmental duplication (Hu et al. 2010; Singh
et al. 2013; Wang et al. 2013b). In addition, although some duplicated genes lose their
function throughout evolution, in P. trichocarpa and other species, it appears that a
majority of the NAC genes generated by gene duplication have been retained by substantial subfunctionalization (Shang et al. 2013). With advances in genome sequencing and assembly techniques, an increase in the availability of full genome sequences
from gymnosperm species and primitive vascular plants is enabling a further understanding of genome evolution across all plant linages. Recently, the draft genome
sequence of Gnetum montanum, a gymnosperm species of gnetophytes, has been
reported, and five NAC genes corresponding to the VNS group were identified. The
authors proposed that these genes are orthologs of VND4/5/6 from Arabidopsis and
VND genes from gymnosperms, suggesting that the vessel-like water-conducting cells
present in Gnetum are morphologically closer to conifer tracheids than to angiosperm
vessels (Wan et al. 2018).
4 Regulation and Mechanism of Action of NAC Proteins
NAC proteins interact with many different types of proteins, including viral proteins,
E3 ubiquitin ligases, phosphatases and kinases, using both their NAC and C-terminal
domains (Welner et al. 2016). In addition, they activate or repress the expression
of their target genes by binding to cis-regulatory elements named NAC recognition
sequences (NACRS), whose consensus sequence varies depending on the NAC
protein. NAC TFs that are involved in stress responses and senescence bind to a
promoter region containing the CACG core DNA-binding motif. Other sequences,
with GCTT or CA(A/C)G(T/C) (T/C/A)(T/C/A) as a core-binding motif, have been
reported as NAC-binding sites (Kim et al. 2007a; Wang et al. 2017). One of the best
characterized sequences to which NAC TFs are attached is a common cis-acting element
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M. B. Pascual et al.
such as SOG1 (SUPPRESSOR OF GAMMA RESPONSE 1) (Yoshiyama 2016) and
with vascular development such as SND2 (SECONDARY WALL-ASSOCIATED
NAC DOMAIN PROTEIN 2) and SND3 involved in secondary cell wall formation.
The identification of NAC TFs in this group of green algae could suggest an essential
role for NAC proteins in protecting the cell against the stresses associated with the
adaptation of plants to a terrestrial environment (Maugarny-Calès et al. 2016).
If the number of NAC genes present in different species is compared throughout
evolution, an expansion of the NAC TF family is observed after the divergence of
tracheophytes. This expansion appears to have arisen through gene duplication or
whole-genome duplication, creating paralogous genes with a high degree of sequence
similarity and functional redundancy (Singh et al. 2013; Wang et al. 2013b). Recent
studies suggest that both tandem and segmental duplication might have played a key role
in the expansion of the NAC family (Puranik et al. 2013; Singh et al. 2013; Wang et al.
2013b; You et al. 2015). In E. grandis, more than 60% of the NAC genes are distributed in tandem in their genome, while in S. tuberosum, V. vinifera and P. trichocarpa,
such expansion has occurred mainly by segmental duplication (Hu et al. 2010; Singh
et al. 2013; Wang et al. 2013b). In addition, although some duplicated genes lose their
function throughout evolution, in P. trichocarpa and other species, it appears that a
majority of the NAC genes generated by gene duplication have been retained by substantial subfunctionalization (Shang et al. 2013). With advances in genome sequencing and assembly techniques, an increase in the availability of full genome sequences
from gymnosperm species and primitive vascular plants is enabling a further understanding of genome evolution across all plant linages. Recently, the draft genome
sequence of Gnetum montanum, a gymnosperm species of gnetophytes, has been
reported, and five NAC genes corresponding to the VNS group were identified. The
authors proposed that these genes are orthologs of VND4/5/6 from Arabidopsis and
VND genes from gymnosperms, suggesting that the vessel-like water-conducting cells
present in Gnetum are morphologically closer to conifer tracheids than to angiosperm
vessels (Wan et al. 2018).
4 Regulation and Mechanism of Action of NAC Proteins
NAC proteins interact with many different types of proteins, including viral proteins,
E3 ubiquitin ligases, phosphatases and kinases, using both their NAC and C-terminal
domains (Welner et al. 2016). In addition, they activate or repress the expression
of their target genes by binding to cis-regulatory elements named NAC recognition
sequences (NACRS), whose consensus sequence varies depending on the NAC
protein. NAC TFs that are involved in stress responses and senescence bind to a
promoter region containing the CACG core DNA-binding motif. Other sequences,
with GCTT or CA(A/C)G(T/C) (T/C/A)(T/C/A) as a core-binding motif, have been
reported as NAC-binding sites (Kim et al. 2007a; Wang et al. 2017). One of the best
characterized sequences to which NAC TFs are attached is a common cis-acting element
204
M. B. Pascual et al.