3 Classification and Evolution of the NAC Family
3.1 The Family of NAC Proteins
Phylogenetic analyses with NAC proteins from different plant species have shown that
the TFs belonging to this family are involved in different aspects of plant growth,
development and stress responses. They can be classified into different clades, suggesting that evolutionarily related NAC genes could play similar roles (Ooka et al.
2003; Shen et al. 2009; Jensen et al. 2010; Pascual et al. 2015). Most studies of the
NAC TF family have been conducted using only the highly conserved N-terminal
NAC subdomains A to E. A systematic analysis of NAC proteins in Arabidopsis, rice
and soybean classified them into different subgroups (Ooka et al. 2003; Pinheiro et al.
2009), showing a clear relationship between structure and function. Shen et al. (2009)
performed a genome-wide bioinformatics survey of 1,232 NAC proteins from 11 plant
species, including woody plants such as poplar and grapevine, and showed that NAC
proteins can be divided into eight subfamilies, termed NAC-a to NAC-h (Shen et al.
2009). More recently, a phylogenetic analysis of NAC proteins from maritime pine
classified the members of this conifer family into six subfamilies according to those
previously defined by Shen et al. (2009) (Pascual et al. 2015). The clade NAC-a
includes proteins involved in responses to biotic and abiotic stress, and it is the largest
subfamily in all species analysed, accounting for 16–34% of the total NAC proteins.
This group included ATAF1, ATAF2, ANAC019 and ANAC55, which have been
shown to be induced by drought, salinity and ABA and to enhance tolerance to drought
when ectopically overexpressed (Tran et al. 2004). The clade NAC-b includes proteins
with transmembrane motifs in their C-terminal domains that play an important role in
cytokinin signalling during cell division or endoplasmic reticulum stress responses (Kim
et al. 2007b; Silva et al. 2015). NAC proteins associated with secondary cell wall biosynthesis and wood formation are grouped into the clade NAC-c, and the proteins implicated
in organ initiation and differentiation (CUC1/2/3 of Arabidopsis) belong to the NAC-d
subfamily. The NAC-e subfamily includes proteins such as FEZ, which are involved in
the orientation of cell division in root meristem (Willemsen et al. 2008), although very
few proteins of this group have been characterized to date. NAC proteins involved in the
secondary cell wall transcriptional network, such as SND2 and SND3 from Arabidopsis
and PgNAC8 from P. glauca, are grouped in the NAC-g subfamily. OsIDEF2 (IRON
DEFICIENCY-BINDING FACTOR 2) belongs to the NAC-f subfamily, and it regulates iron homeostasis-related genes in rice (Ogo et al. 2008; Shen et al. 2009), and
SENU5 members are included in the NAC-h subfamily, which have been demonstrated to be involved in leaf senescence (Guo and Gan 2006; Shen et al. 2009). No
NAC protein belonging to NAC-f was found in moss (P. patens, bryophyte), spike
moss (Selaginella moellendorffii, lycophyte) or gymnosperms (P. pinaster), and the
clade NAC-h was also absent in P. patens or P. pinaster, suggesting that these two
subfamilies appeared later during evolution and possibly with more specific and
specialized functions.
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M. B. Pascual et al.
3.1 The Family of NAC Proteins
Phylogenetic analyses with NAC proteins from different plant species have shown that
the TFs belonging to this family are involved in different aspects of plant growth,
development and stress responses. They can be classified into different clades, suggesting that evolutionarily related NAC genes could play similar roles (Ooka et al.
2003; Shen et al. 2009; Jensen et al. 2010; Pascual et al. 2015). Most studies of the
NAC TF family have been conducted using only the highly conserved N-terminal
NAC subdomains A to E. A systematic analysis of NAC proteins in Arabidopsis, rice
and soybean classified them into different subgroups (Ooka et al. 2003; Pinheiro et al.
2009), showing a clear relationship between structure and function. Shen et al. (2009)
performed a genome-wide bioinformatics survey of 1,232 NAC proteins from 11 plant
species, including woody plants such as poplar and grapevine, and showed that NAC
proteins can be divided into eight subfamilies, termed NAC-a to NAC-h (Shen et al.
2009). More recently, a phylogenetic analysis of NAC proteins from maritime pine
classified the members of this conifer family into six subfamilies according to those
previously defined by Shen et al. (2009) (Pascual et al. 2015). The clade NAC-a
includes proteins involved in responses to biotic and abiotic stress, and it is the largest
subfamily in all species analysed, accounting for 16–34% of the total NAC proteins.
This group included ATAF1, ATAF2, ANAC019 and ANAC55, which have been
shown to be induced by drought, salinity and ABA and to enhance tolerance to drought
when ectopically overexpressed (Tran et al. 2004). The clade NAC-b includes proteins
with transmembrane motifs in their C-terminal domains that play an important role in
cytokinin signalling during cell division or endoplasmic reticulum stress responses (Kim
et al. 2007b; Silva et al. 2015). NAC proteins associated with secondary cell wall biosynthesis and wood formation are grouped into the clade NAC-c, and the proteins implicated
in organ initiation and differentiation (CUC1/2/3 of Arabidopsis) belong to the NAC-d
subfamily. The NAC-e subfamily includes proteins such as FEZ, which are involved in
the orientation of cell division in root meristem (Willemsen et al. 2008), although very
few proteins of this group have been characterized to date. NAC proteins involved in the
secondary cell wall transcriptional network, such as SND2 and SND3 from Arabidopsis
and PgNAC8 from P. glauca, are grouped in the NAC-g subfamily. OsIDEF2 (IRON
DEFICIENCY-BINDING FACTOR 2) belongs to the NAC-f subfamily, and it regulates iron homeostasis-related genes in rice (Ogo et al. 2008; Shen et al. 2009), and
SENU5 members are included in the NAC-h subfamily, which have been demonstrated to be involved in leaf senescence (Guo and Gan 2006; Shen et al. 2009). No
NAC protein belonging to NAC-f was found in moss (P. patens, bryophyte), spike
moss (Selaginella moellendorffii, lycophyte) or gymnosperms (P. pinaster), and the
clade NAC-h was also absent in P. patens or P. pinaster, suggesting that these two
subfamilies appeared later during evolution and possibly with more specific and
specialized functions.
202
M. B. Pascual et al.