Grass Flowers: an Untapped Resource for Floral Evo-Devo
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Journal of Systematics JSE and Evolution doi: 10.1111/jse.12251 Review Grass flowers: An untapped resource for floral evo-devo Amanda Schrager-Lavelle1, Harry Klein1, Amanda Fisher2, and Madelaine Bartlett1* 1Biology Department, University of Massachusetts, Amherst, MA 01003, USA 2Biological Sciences Department, California State University, Long Beach, CA 90840, USA *Author for correspondence. E-mail: [email protected] Received 14 February 2017; Accepted 27 March 2017; Article first published online xx Month 2017 Abstract The abrupt origin and rapid diversification of the flowering plants presents what Darwin called “an abominable mystery”. Floral diversification was a key factor in the rise of the flowering plants, but the molecular underpinnings of floral diversity remain mysterious. To understand the molecular biology underlying floral morphological evolution, genetic model systems are essential for rigorously testing gene function and gene interactions. Most model plants are eudicots, while in the monocots genetic models are almost entirely restricted to the grass family. Likely because grass flowers are diminutive and specialized for wind pollination, grasses have not been a major focus in floral evo-devo research. However, while grass flowers do not exhibit any of the raucous morphological diversification characteristic of the orchids, there is abundant floral variation in the family. Here, we discuss grass flower diversity, and review what is known about the developmental genetics of this diversity. In particular, we focus on three aspects of grass flower evolution: (1) the evolution of a novel organ identity—the lodicule; (2) lemma awns and their diversity; and (3) the convergent evolution of sexual differentiation. The combination of morphological diversity in the grass family at large and genetic models spread across the family provides a powerful framework for attaining deep understanding of the molecular genetics of floral evolution. Key words: awns, evolution of plant development, evolutionary developmental biology, floral sexuality, flower development, flower evolution. 1 Model Systems for Mechanistic Under- et al., 2016). Although both candidate gene and comparative standing gene expression studies have been fruitful (e.g., Bharathan et al., 2002; Whipple et al., 2007; Yang et al., 2014), on their The evolution of the flower approximately 140 million years own, neither can reveal the precise mechanistic detail of the ago (Magallon et al., 2015) was a critical event in the history of molecular evolution underlying morphological evolution. In terrestrial ecosystems. Flowers display fantastic diversity in addition, both candidate gene and comparative gene form. Selection for pollination success—through intricate plant/insect interactions or optimized abiotic pollination—has likely been critical in shaping floral morphological diversity (Fenster et al., 2004; Friedman & Barrett, 2008). Probing floral Terminology Anthesis, Time at which a flower is open and releasing pollen and/or diversity in an evo-devo framework allows one to ask pollen receptive. questions about, for example, the evolution of novelty, fi Awn, A narrow appendage that is an extension of the vascular morphological diversi cation, and the convergent evolution tissue; can be simple or branched. of plant form and function (Endress, 2011; Glover et al., 2015; Cleistogamous, Self-fertilization without the flower opening. Specht & Howarth, 2015). Thus, floral evolution represents an Diaspore,A‘unit of dispersal’; the seed and enclosing and attached obvious arena for plant evo-devo. structures. Despite some significant inroads (reviewed in Glover et al., Dicliny, Any breeding system that includes unisexual flowers. Dicliny 2015; Specht & Howarth, 2015), mechanistic understanding of includes, for example, monoecy, dioecy, gynodioecy, andromonoecy. the molecular genetics of floral evolution remains elusive in Floret, Reproductive structure in grasses homologous to a single most systems. Many of the systems in which these questions flower in other plants. Contains pistil, stamens, lodicules, palea, and lemma. can be asked—families where floral morphological diversity is Lemma, Outer-most whorl of a grass flower with unknown most spectacular (e.g., the orchids), or the taxa that are most homology. informative in terms of phylogenetic placement (e.g., the Lodicule, Scale-like structures in the grass flower, homologous to — sister to all other angiosperms Amborella trichopoda Baill.), inner whorl tepals. are currently intractable to most experimentation beyond Spikelet, A branch of 1 to several flowers, subtended by a pair of candidate gene studies and comparative gene expression glumes (bracts). experiments, either on a large or small scale (Chanderbali Staminode, Stamen that fails to produce pollen; sterile. XXX 2017 | Volume 9999 | Issue 9999 | 1–17 © 2017 Institute of Botany, Chinese Academy of Sciences 2 Schrager-Lavelle et al. expression studies depend on our understanding of molecular only family with multiple established genetic model systems in gene function obtained from model genetic systems. Vast the monocots is the grass family (Poaceae). The grass family evolutionary distances often separate the dominant model includes four more-or-less established model systems—Zea system, Arabidopsis thaliana (L.) Heynh. (arabidopsis), from mays L. (maize), Oryza sativa L. (rice), Brachypodium those species most interesting to floral biologists. Conserved distachyon (L.) P. Beauv., and Setaria viridis Beauv. (Setaria). gene function cannot be assumed over 100þ million years of Each of these systems is transformable, has a fully sequenced evolution, and fine-grained hypotheses about changes in gene genome, and either a very well-established or growing function are very difficult to test rigorously without the collection of genetic resources and tools available (Goff molecular genetic tools available in model systems (Becker et al., 2002; Strable & Scanlon, 2009; Brutnell et al., 2010; et al., 2011; Chanderbali et al., 2016). It is possible to test some Brkljacic et al., 2011). CRISPR/Cas9 genome editing has been aspects of gene function through heterologous transforma- demonstrated in maize, rice and B. distachyon (Miao et al., tion of arabidopsis, but it is very difficult to draw substantive 2013; Svitashev et al., 2015; Raissig et al., 2016), and Setaria is conclusions using distantly related heterologous systems likely not far behind. In addition, there are a number of (Kramer, 2015). Identifying quantitative trait loci (QTL) within emerging systems that are being developed, and several species can yield substantial insight into the genetic under- cereal crops (e.g., barley (Hordeum vulgare L.), wheat pinnings of diversity, but QTL studies can only be used to study (Triticum aestivum L.), sorghum (Sorghum bicolor (L.) traits that vary at the species level (Mauricio, 2001). Moench)) have established research communities and a Macroevolutionary traits that are often of the most interest growing body of knowledge (reviewed in Chang et al., 2016). to floral biologists (e.g., the evolution of novel organs) are We argue that this powerful genetic framework can be usually consistent within genera, and vary at deeper fruitfully leveraged for mechanistic understanding of floral evolutionary levels (Endress, 2011). Thus, precisely connecting evo-devo. molecular evolution to floral morphological evolution remains challenging without access to the resources of an established model system. Multiple model systems in single lineages (orders, families, 2 A Primer of Grass Flower Morphology genera) hold the most promise for detailed insight into the Grass flowers are usually wind pollinated, although there are evolutionary molecular genetics of development above the some reports of insect visitors (Soderstrom et al., 1971; Huang species level (Chanderbali et al., 2016; Damerval & Becker, et al., 2002; Sajo et al., 2009; Ruiz-Sanchez et al., 2017) and 2017). This has been clearly illustrated in the Brassicaceae, they exhibit a number of features typical of wind-pollinated where functional comparisons between arabidopsis and plants (Fig. 1). They are small, lack showy petals, usually exsert Cardamine hirsuta L. have led to significant insights into the their anthers on long, thin filaments, and typically have molecular evolution underlying leaf and fruit form (Hay & feathery stigmas. Unisexuality, often associated with wind Tsiantis, 2006; Vlad et al., 2014; Hofhuis et al., 2016). In the pollination, has evolved multiple times in the grasses, eudicots, the Brassicaceae and Ranunculaceae each include although unisexuality is still not common among the multiple established or emerging systems that vary in key approximately 11,000 species in the family (Friedman & morphological traits (Kramer, 2009; Canales et al., 2010; Barrett, 2008; Kinney et al., 2008). Damerval & Becker, 2017). Studies in these systems allow for The structure of grass flowers has been very recently and the precise dissection of gene function and for making strong expertly reviewed (Kellogg, 2015), so we will only discuss connections between molecular and morphological evolution aspects of the flower relevant to our discussion. A glossary of (e.g., Sharma & Kramer, 2013; Vlad et al., 2014). some specialized terminology is included on the first page. The monocots represent 24% of angiosperm diversity, and Grass flowers or florets develop in groups of 1–150, clustered are characterized by a number of speciose, extremely on short branches called