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Review
. 2024 May 14;25(10):5369.
doi: 10.3390/ijms25105369.

Transcriptional Control of Seed Life: New Insights into the Role of the NAC Family

Javier Fuertes-Aguilar  1 , Angel J Matilla  2
Affiliations
Review

Transcriptional Control of Seed Life: New Insights into the Role of the NAC Family

Javier Fuertes-Aguilar et al. Int J Mol Sci. .

Abstract

Transcription factors (TFs) regulate gene expression by binding to specific sequences on DNA through their DNA-binding domain (DBD), a universal process. This update conveys information about the diverse roles of TFs, focusing on the NACs (NAM-ATAF-CUC), in regulating target-gene expression and influencing various aspects of plant biology. NAC TFs appeared before the emergence of land plants. The NAC family constitutes a diverse group of plant-specific TFs found in mosses, conifers, monocots, and eudicots. This update discusses the evolutionary origins of plant NAC genes/proteins from green algae to their crucial roles in plant development and stress response across various plant species. From mosses and lycophytes to various angiosperms, the number of NAC proteins increases significantly, suggesting a gradual evolution from basal streptophytic green algae. NAC TFs play a critical role in enhancing abiotic stress tolerance, with their function conserved in angiosperms. Furthermore, the modular organization of NACs, their dimeric function, and their localization within cellular compartments contribute to their functional versatility and complexity. While most NAC TFs are nuclear-localized and active, a subset is found in other cellular compartments, indicating inactive forms until specific cues trigger their translocation to the nucleus. Additionally, it highlights their involvement in endoplasmic reticulum (ER) stress-induced programmed cell death (PCD) by activating the vacuolar processing enzyme (VPE) gene. Moreover, this update provides a comprehensive overview of the diverse roles of NAC TFs in plants, including their participation in ER stress responses, leaf senescence (LS), and growth and development. Notably, NACs exhibit correlations with various phytohormones (i.e., ABA, GAs, CK, IAA, JA, and SA), and several NAC genes are inducible by them, influencing a broad spectrum of biological processes. The study of the spatiotemporal expression patterns provides insights into when and where specific NAC genes are active, shedding light on their metabolic contributions. Likewise, this review emphasizes the significance of NAC TFs in transcriptional modules, seed reserve accumulation, and regulation of seed dormancy and germination. Overall, it effectively communicates the intricate and essential functions of NAC TFs in plant biology. Finally, from an evolutionary standpoint, a phylogenetic analysis suggests that it is highly probable that the WRKY family is evolutionarily older than the NAC family.

Keywords: TF binding sites; WRKY and NAC families; endoplasmic reticulum; endosperm; phytohormones; seed dormancy and germination.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
TFs exhibit characteristic domains responsible for various functions, including DNA binding, oligomerization/protein–protein interactions, transcriptional regulation, and nuclear localization. The accompanying figure illustrates the structure of a NAC-TF. The NAC domain, enclosed by a red ellipse, comprises nearly 150 amino acid residues and often includes a nuclear localization signal, enabling protein binding. Subdomain A facilitates protein dimerization, subdomains B and E contribute to functional diversity, while subdomains C and D, which are positively charged and highly conserved, are responsible for DNA binding. The C-terminal transcriptional regulatory (TR) region, surrounded by a green ellipse, functions as a transcriptional activator or repressor and may possess protein binding activity, interacting with other TFs. Adapted from Singh [33] and Diao [57].
Figure 2
Figure 2
The cellular synthesis of NACs generates a population of these TFs in the ER. The nuclear genes responsible are affected by phytohormones. A notable portion of the NAC population is sent to the nucleus to alter the transcription of target genes, producing the corresponding proteins. These proteins alter a series of physiological processes such as LS, seed reserve degradation (e.g., starch), ER stress, and seed dormancy and germination, among others. The remaining endoplasmic population of NACs (membrane-tethered NAC TFs) is sent to cellular compartments (i.e., chloroplasts, peroxisomes, and mitochondria) and plasma membranes. The membrane-tethered subset is a small family specific to plants, which lose their transmembrane domain and are then sent to the nucleus to exert their physiological role once bound to the corresponding target genes. The exit of membrane-tethered NAC TF from the corresponding cellular compartment occurs in response to environmental and developmental changes. For further information, see [71,76,77].
Figure 3
Figure 3
Maximum-Likelihood phylogenetic analysis of 266 NAC and 268 WRKY protein sequences, aligned with ClustalW, performed in IQ-TREE (2021) under a JTT + R7 model chosen according to BIC. Red diamond indicates the node (BS 85%) showing a sister relationship between WRKY group 1 and NAC genes. White circles designate main groups of NAC genes following Pereira Santana et al. (2015) [251], and WRKY genes according to Zhang and Wang (2005) [247].
Figure 4
Figure 4
This tree indicates that Klebsomidiales is the last lineage without NAC TFs, while Charales is the first lineage with WRKY and NACs. For each species, the habitat and documented occurrence of WRKY and NAC gene families are depicted. Adapted from Leebens-Mack et al. 2019 [252] and Wang et al. 2021 [253].
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References

    1. Martínez-Ainsworth N.E., Tenaillon M.I. Superheroes and masterminds of plant domestication. C. R. Biol. 2016;339:268–273. doi: 10.1016/j.crvi.2016.05.005. - DOI - PubMed
    1. Chowdhary A.A., Mishra S., Mehrotra S., Upadhyay S.K., Bagal D., Srivastava V. Plant transcription factors: An overview of their role in plant life. Plant Transcr. Factors. 2023:3–20. doi: 10.1016/B978-0-323-90613-5.00003-0. - DOI
    1. Ding Y., Zhu J., Zhao D., Liu Q., Yang Q., Zhang T. Targeting cis-regulatory elements for rice grain quality improvement. Front. Plant Sci. 2021;12:70583. doi: 10.3389/fpls.2021.705834. - DOI - PMC - PubMed
    1. Liu S., Guan Y., Weng Y., Liao B., Tong L., Hao Z., Chen J., Shi J., Cheng T. Genome-wide identification of the NAC gene family and its functional analysis in Liriodendron. BMC Plant Biol. 2023;23:415. doi: 10.1186/s12870-023-04415-4. - DOI - PMC - PubMed
    1. Rui Z., Pan W., Zhao Q., Hu H., Li X., Xing L., Jia H., She K., Nie X. Genome-wide identification, evolution and expression analysis of NAC gene family under salt stress in wild emmer wheat (Triticum dicoccoides L.) Int. J. Biol. Macromol. 2023;230:12337. doi: 10.1016/j.ijbiomac.2023.123376. - DOI - PubMed

Grants and funding

Javier Fuertes-Aguilar’s (J.F.-A.) research was funded by NEXTPOL project grant PGC2018-100684-B-I00, Spanish Ministry of Science and Innovation.