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Evolution of Angiosperm Pollen. 7. Nitrogen-Fixing Clade1 Evolution of Angiosperm Pollen. 7. Nitrogen-Fixing Clade1 Authors: Jiang, Wei, He, Hua-Jie, Lu, Lu, Burgess, Kevin S., Wang, Hong, et. al. Source: Annals of the Missouri Botanical Garden, 104(2) : 171-229 Published By: Missouri Botanical Garden Press URL: https://doi.org/10.3417/2019337 BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-of-use. Usage of BioOne Complete content is strictly limited to personal, educational, and non - commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Downloaded From: https://bioone.org/journals/Annals-of-the-Missouri-Botanical-Garden on 01 Apr 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by Kunming Institute of Botany, CAS Volume 104 Annals Number 2 of the R 2019 Missouri Botanical Garden EVOLUTION OF ANGIOSPERM Wei Jiang,2,3,7 Hua-Jie He,4,7 Lu Lu,2,5 POLLEN. 7. NITROGEN-FIXING Kevin S. Burgess,6 Hong Wang,2* and 2,4 CLADE1 De-Zhu Li * ABSTRACT Nitrogen-fixing symbiosis in root nodules is known in only 10 families, which are distributed among a clade of four orders and delimited as the nitrogen-fixing clade. As the seventh in a series that examines pollen morphological distribution and evolution in the angiosperms, this paper focuses on pollen morphological character states of the nitrogen-fixing clade. To illustrate the palynological diversity of the clade, we first examined pollen grains from 26 species with light electron, scanning electron, and transmission electron microscopy. Second, we used a reduced data matrix from Li et al. (2015) to reconstruct a maximum likelihood tree and then optimized 18 pollen character states onto the tree using Fitch parsimony, maximum likelihood, and hierarchical Bayesian inference. Finally, 12 plesiomorphic states for the nitrogen-fixing clade were inferred unambiguously under all methods, and more than 40 clades (or lineages) at or above familial level were characterized by unambiguous pollen character state changes in at least one of the optimizations. We found a number of evolutionary trends for changes in pollen character states. These include increasing grain size, increasing aperture number accompanied by concomitant changes in aperture position (from equatorial to global) and aperture shape (from colpate to colporate), and increasing complexity of tectum ornamentation. There was a strong correlation between some pollen characters (prolate shape class, lobe outline in polar view, colpate ectoaperture, lalongate and lolongate endoaperture, absent supratectal element, reticulate tectum) and insect pollination, while other pollen characters—simple aperture structure, porate ectoaperture, circular endoaperture, present and gemmate or echinate supratectal element, and 1 We thank Dr. Alexandra H. Wortley and Prof. Stephen Blackmore from Royal Botanic Garden Edinburgh for their kind help with earlier versions of the manuscript, Dr. Z. X. Ren for collecting pollen samples and helping with pollen observations under SEM, and Dr. M. Y. Zhang for her suggestions on data analysis. We are also grateful to Kunming Institute of Botany Herbarium (KUN), Royal Botanic Garden Edinburgh Herbarium (E), Australian National Herbarium (CANB), and Xishuangbanna Tropical Botanical Garden Herbarium (XTBG) for providing pollen samples. This study was supported by grants from the Major International Joint Research Project of the National Natural Science Foundation of China (no. 31320103919), National Natural Science Foundation of China (no. 31270272), and the Keynote Project of National Natural Science Foundation of China (no. 40830209). 2 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, CAS, Kunming 650201, People’s Republic of China. 3 The Industrial Crops Research Institute, Yunnan Academy of Agricultural Sciences, Kunming, 650200, People’s Republic of China. 4 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, CAS, Kunming 650201, People’s Republic of China. 5 School of Pharmaceutical Sciences and Yunnan Key Laboratory of Pharmacology for Natural Products, Kunming Medical University, Kunming, 650500, People’s Republic of China. 6 Department of Biology, College of Letters & Sciences, Columbus State University, University System of Georgia, Columbus, Georgia 31907, U.S.A. 7 These authors contributed equally to this work. * Authors for correspondence: [email protected]; [email protected] VERSION OF RECORD FIRST PUBLISHED ONLINE ON 11 JUNE 2019 AHEAD OF SUMMER 2019 ISSUE. – Downloaded From:doi: https://bioone.org/journals/Annals-of-the-Missouri-Botanical-Garden 10.3417/2019337 ANN on.M 01 AprISSOURI 2020 BOT.GARD. 104: 171 229. Terms of Use: https://bioone.org/terms-of-use Access provided by Kunming Institute of Botany, CAS 172 Annals of the Missouri Botanical Garden imperforate tectum—were strongly correlated with wind pollination. In addition, rugulate tectum was significantly correlated with shrub habit while larger pollen size was significantly correlated with vine habit; the helophytic habitat was significantly correlated with having two apertures. Our study provides rich evidence for the phylogenetic significance of pollen morphological diversity in the nitrogen-fixing clade. Key words: Character evolution, Cucurbitales, Fabales, Fagales, nitrogen-fixing clade, pollen morphology, Rosales, systematic significance. This study, the seventh in a series investigating Within Rosales, the families Rhamnaceae, Elaeag- pollen character state distribution and evolution across naceae, Barbeyaceae, and Dirachmaceae seem to form the angiosperms in a phylogenetic context, examines the a clade, but relationships within the clade remain diversity of pollen character states in the nitrogen-fixing unresolved. Although a close relationship between clade (Fig. 1). The nitrogen-fixing clade lies within the Rhamnaceae and Elaeagnaceae was reconstructed, the rosids, and the clade is commonly divided into four finding may be due to a lack of sampling for the other two orders: Cucurbitales, Fabales, Fagales, and Rosales families (Wang et al., 2009; Soltis et al., 2011). Some (Soltis et al., 1995), together comprising 28 families, studies have placed the Rhamnaceae as basally branch- approximately 1170 genera, and more than 30,000 ing, with Dirachmaceae and Barbeyaceae forming species (Magallon et al., 1999; Soltis et al., 2005; a clade with Elaeagnaceae (Zhang et al., 2011), while APG IV, 2016). The nitrogen-fixing clade exhibits other studies place Barbeyaceae and Elaeagnaceae enormous heterogeneity in habit, habitat, and life form as weakly supported sister groups, together forming (Soltis et al., 2005), but its most noticeable character- a clade with Rhamnaceae, but Dirachmaceae is the istic is the high number of rhizobial and actinorhizal basal branch (Xiang et al., 2014; Li et al., 2015; Sun plants bearing root nodules that contain nitrogen-fixing et al., 2016). Similarly, relationships within Cucurbi- bacteria, which give these taxa a competitive advantage tales remain unclear except for a firm sister group in nutrient-deficient soils (Soltis et al., 1995; Biswas & relationship between Coriariaceae and Corynocarpa- Gresshoff, 2014; Mus et al., 2016). The clade contains ceae. A clade comprising Datiscaceae and Begoniaceae many economically important families including le- receives at best only moderate support (Zhang et al., gumes (Fabaceae), gourds (Cucurbitaceae), fruit crops 2006; Schaefer et al., 2009; Schaefer & Renner, (Rosaceae), and temperate and tropical forest trees 2011b), and a possible relationship between Tetrame- (e.g., Betulaceae, Cannabaceae, Fabaceae, Fagaceae, laceae and Datiscaceae has also been recovered by and Ulmaceae; Wang et al., 2009). Swensen et al. (1994), Li et al. (2015), and Sun et al. Most previous studies agree on both the composition (2016). In contrast to the lack of family resolution within of the nitrogen-fixing clade and the relationships among the other three orders within this clade, relationships its four orders, with Fabales being the most basally within Fagales are well resolved except for the position branching, Rosales the next diverging, and Fagales and of Myricaceae, which has been placed as sister group to Cucurbitales forming sister groups (Wang et al., 2009; Casuarinaceae–(Ticodendraceae–Betulaceae) (Sauquet Soltis et al., 2011; Li et al., 2015; Sun et al., 2016). et al., 2012; Xiang et al., 2014; Xing et al., 2014; Deep relationships within orders, however, remain Li et al., 2015; Sun et al., 2016), or to Juglandaceae poorly understood (APG I, 1998; APG II, 2003; (Li et al., 2004, 2016; Larson-Johnson, 2016). APG III, 2009; APG IV, 2016); in particular, the The potential of palynological characters to sup- resolution of several families remains ambiguous. port systematic classifications has been discussed by For example,
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