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Gymnosperm Welwitschia Provides New Insights Into the Origin of Flowers

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Gymnosperm Welwitschia Provides New Insights Into the Origin of Flowers Journal of Experimental Botany, Vol. 69, No. 23 pp. 3–15, 2018 doi:10.1093/jxb/ery120 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) Flowering Highlights A miraculous mirabilis: the gymnosperm Welwitschia provides new insights into the origin of flowers Frank Wellmer Smurfit Institute of Genetics, Trinity College Dublin, Ireland [email protected] The specification of male and female reproductive organs in gymnosperms and angiosperms is thought to be remarkably similar and to depend on the activities of B and C class MADS domain transcription factors. When B and C class factors Welwitschia mirabilis plants are co-expressed, male organs are formed, while C class activity alone leads to growing east of Swakopmund the development of female organs. It has been shown that the expression of (Namibia). Image courtesy of Steve Weller. gymnosperm B and C class genes can rescue the developmental defects of floral mutants, in which the homologous organ identity genes are disrupted (Zhang et al., 2004). Thus, it appears that the biochemical activities of the corresponding transcription factors have largely remained unchanged since the two groups of seed bearing plants diverged around 150 million years ago. Despite these similarities, it is not known how in angiosperms male and female organs became part of the same reproductive unit (i.e. the flower), while in gymnosperms they are separated in unisexual structures (e.g. male and female cones). It has been proposed that changes in the expression patterns of B and/ or C function genes, leading to partially overlapping domains of expression and activity, were crucial to the origin of bisexual flowers. However, how these changes may have been brought about is currently not known. To address this question, detailed knowledge on the regulation of B and C class genes in both gymnosperms and angiosperms is required. While over the past 25 years the regulation of floral organ identity genes has been extensively studied, especially in the model angiosperm Arabidopsis thaliana, little is known about how the expression of © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. orthologous genes in gymnosperms is controlled. A recent study using Welwitschia mirabilis addressed this knowledge gap and provided molecular evidence for the regulation of B class genes by the plant-specific transcription factor LEAFY (LFY) (Moyroud et al., 2017). LFY has previously been shown to be pivotal for triggering the expression of floral organ identity genes during early flower development in Arabidopsis (Busch et al., 1999; Parcy et al., 1998). In contrast to extant angiosperms, which possess a single LFY gene, gymnosperms typically have two LFY paralogs, one that is LFY-like and one termed NEEDLY (NDLY) or NDLY-like (Frohlich and Parker, 2000). It thus appears that early on during their evolution, angiosperms lost the NDLY-like gene and retained only the gene that is LFY-like. It is attractive to speculate that this change in the complement of known key regulators of B and C class genes may have been a crucial step in the evolution of flowers. However, what are the functions of the LFY and NDLY transcription factors in gymnosperms and how similar are they to those of LFY in angiosperms? To answer these questions, Moyroud and colleagues first characterized the expression of LFY, NDLY as well as of likely B and C class genes in developing male cones of Welwitschia. They found that the expression of both LFY and NDLY precedes or parallels that of the organ identity genes as would be expected if the corresponding transcription factors were involved, as LFY in angiosperms, in activating the expression of B and C class genes. Furthermore, they observed that at later stages of male cone development the expression of LFY and B class genes was noticeably different to that of NDLY and the C class gene under study. Thus, based on the expression patterns of these genes alone, it can be hypothesized that LFY may control B class genes, while NDLY might be involved in the control of C class gene activity. In support of this idea, Moyroud et al. (2017) using advanced biochemical and biophysical techniques showed that LFY and NDLY have overlapping but distinct sets of binding sites. They further demonstrated that LFY from Welwitschia as well as from other gymnosperms can bind to putative regulatory elements in the promoters of B class genes. Therefore, it seems that LFY in both gymnosperms and angiosperms plays a key role in the control of these organ identity genes. While the molecular activities of NDLY need to be further characterized, the study by Moyroud and colleagues led to the attractive and testable hypothesis that this transcription factor may not share all functions with its paralog LFY and might control C class gene activity in gymnosperms. References Busch MA, Bomblies K, Weigel D. 1999. Activation of a floral homeotic gene in Arabidopsis. Science 285, 585–587. Frohlich MW, Parker DS. 2000. The mostly male theory of flower evolutionary origins: from genes to fossils. Systematic Botany 25, 155–170. Moyroud E, Monniaux M, Thévenon E, Dumas R, Scutt CP, Frohlich MW, Parcy F. 2017. A link between LEAFY and B-gene homologues in Welwitschia mirabilis sheds light on ancestral mechanisms prefiguring floral development. New Phytologist216 , 469–481. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D. 1998. A genetic framework for floral patterning. Nature 395, 561–566. Zhang P, Tan HT, Pwee KH, Kumar PP. 2004. Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. The Plant Journal 37, 566–577..
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