April 4, 2014

Review: Contribution of NAC transcription factors to plant adaptation to land

March 20 2014 Science 28 March 2014: Vol. 343 no. 6178 pp. 1505-1508
DOI: 10.1126/science.1248417

Bo Xu1, Misato Ohtani2, Masatoshi Yamaguchi1, Kiminori Toyooka2, Mayumi Wakazaki2, Mayuko Sato2, Minoru Kubo3, Yoshimi Nakano1, Ryosuke Sano1, Yuji Hiwatashi3, Takashi Murata3, Tetsuya Kurata1, Arata Yoneda1, Ko Kato1, Mitsuyasu Hasebe3,4, Taku Demura1,2,*
* Corresponding author

1Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara 630-0192, Japan.
2RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230-0045, Japan.
3National Institute for Basic Biology, Okazaki, Aich 444-8585, Japan.
4School of Life Science, Graduate University for Advanced Studies, Okazaki, Aich 444-8585, Japan.

The colonization of land by early plants required the evolution of two specialized features which were not necessary for life in an aquatic environment: water-conducting tissues and support structures. Japanese researchers lead by Prof. Taku Demura of the RIKEN Center recently reported that the evolution of a family of transcription factors known as NO APICAL MERISTEM (NAC) may indeed have been responsible for the acquisition of both structures1. Although most current information on the evolution and function of water-conducting elements comes from studies using Arabidopsis2-4, the well characterized moss Physcomitrella patens is a valuable model system which frequently provides insights of how early plant evolution may have taken place.

It had been previously suggested from Arabidopsis studies that both fiber cells and xylem vessels share an evolutionary origin5, and in modern vascular plants these structures have functions in support and water transport, respectively. In moss, the homologous structures are known as stereids and hydroids. In the present work, Xu et al. characterize the regulation of NAC transcription factors in Physcomitrella (here referred to as PpVNS proteins, which include VDN [VASCULAR RELATED NAC-DOMAN], NST [NAC SECONDARY WALL THICKENING PROMOTING FACTOR], and SMB [SOMBRERO-related] and examine their role in the development in stereid and hydroid cell types. The evolutionary link between NAC transcription factors in bryophytes and flowering plants is not obvious since xylem vessels and fiber cells are only produced during the sporophytic generation of vascular plants, while the homologous stereids and hydroids of mosses are only present in the gametophytic generation.

Using qRTPCR on gametophyte and protonemata tissues, GUS-staining of transformed moss lines and anatomical evaluation of ppvns knock-out mutants, Xu et al. established PpVNS1, 6, and 7 as proteins with critical roles in the development of both hydroids and stereids in the gametophyte leaf, whereas PpVNS4 controls development of hydroids in the gametophyte stem (and to a lesser extent, central and transfer cells in the sporophyte foot). Mutants defective in one or more PpVNS gene displayed reduced capacity to conduct water, an enhanced sensitivity to wilting, and reduced stereid cell wall thickness. Unlike stereids of wild type plants, those of ppvns triple mutants retained their cellular contents, including plastids. Overexpression of PpVNS proteins using an inducible promoter provoked cell death, chloroplast loss, and protoplasm shrinkage in hydroids. This effect was also seen when moss was transformed with an Arabidopsis NAC protein (VDN7), which further established the evolutionary link between the homologous genes of bryophyte and flowering plants. When Arabidopsis was transformed with PpVNS proteins, ectopic secondary wall thickening was observed. 

Together, the authors present a powerful argument for the role of these NAC proteins in the functionalization of both support cells and water conducting vessels by promoting cell wall thickening (in stereids) and clearance of cellular contents (in hydroids). Because the conductivity of water is much more efficient in dead, empty cells than in living parenchyma cells with normal cellular contents, the evolution of the cell death program may well have facilitated the evolution of water conduction. Without the latter, the colonization of land by aquatic plants was all but impossible. Indeed, the evolution of this family of transcription factors may have been a key innovation that allowed early plants not only to colonize land but also to evolve large, complex body types with increased requirements for water transport. The authors are congratulated on this important advance in our understanding of the role of these proteins in support and water-conducting cells types both in bryophytes as well as in vascular plants.Additionally, this study provides new insights into how evolution may proceed with major ecological consequences, such as adaptation of an entire group of organisms to a new habitat, brought about by the simple innovation of extant transcription factors.

Questions: This work prompts many questions regarding the evolution of NAC proteins and mode of action in vascular plants. What is the phylogenetic relationship between NACs of Physcomitrella and Arabidopsis? Has this group of transcription factors acquired any new functions during the evolution of angiosperms or are they always related to the development of either fibers of xylem vessels? How precisely do NAC transcription factors induce cell death, e.g. what are their primary targets and which transcripts are the first to be activated towards this end? Are there any obvious biotechnological applications which these new insights into NAC protein function might provide?

1.         Xu, B. et al. Contribution of NAC transcription factors to plant adaptation to land. Science 343, 1505-1508 (2014).
2.         Kubo, M. et al. Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19, 1855-1860 (2005).
3.         Ohashi-Ito, K., Oda, Y. & Fukuda, H. Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22, 3461-3473 (2010).
4.         Yamaguchi, M. et al. VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153, 906-914 (2010).
5.         Zhong, R., Demura, T. & Ye, Z.-H. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18, 3158-3170 (2006).

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