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<I>Solidago Houghtonii</I

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<I>Solidago Houghtonii</I Systematic Botany (2011), 36(1): pp. 209–226 © Copyright 2011 by the American Society of Plant Taxonomists DOI 10.1600/036364411X553289 Nuclear and Chloroplast DNA Suggest a Complex Single Origin for the Threatened Allopolyploid Solidago houghtonii (Asteraceae) Involving Reticulate Evolution and Introgression Pamela J. Laureto 1 and Todd J. Barkman Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 U. S. A. 1 Current address: Department of Biological Sciences, Grand Rapids Community College, Grand Rapids, Michigan 49503 U. S. A. 1 Author for correspondence ([email protected]) Communicating Editor: Andrew Hipp Abstract— Solidago houghtonii Torrey & A. Gray ex Gray is a federally threatened polyploid plant species likely of hybrid origin. Several hypothesized combinations of parental species have been suggested but none have been phylogenetically tested. Additionally, it is unclear whether the species is of single or polytopic origin. To study the evolutionary history of S. houghtonii we sequenced four noncoding cpDNA loci ( accD-psaI , psbA-trnH , trnL-trnF , rps16-trnQ ), and the ITS and 3′ETS regions for four accessions of S. houghtonii , which span its geographic range, and 25 other species of Solidago including all sympatric species. Polymorphisms within the direct nrDNA sequences of all S. houghtonii accessions indicated the presence of multiple homoeologue types. These were separated by molecular cloning of the 3055 bp 3′ETS – ITS region, allowing us to positively link the ETS and ITS homoeologue types. Phylogenetic analyses of the nuclear and chloroplast datasets revealed incongruent topologies. Analysis of cloned nrDNA sequence data indicated that S. riddellii, S. ptarmicoides , and S. ohioensis have contributed to the nuclear genome of S. houghtonii. Analysis of cpDNA sequence data revealed the presence of multiple insertions/deletions that are shared by all accessions. The unique pattern of cpDNA indels was also recovered in S. gigantea . Phylogenetic analysis of the cpDNA sequence data and coded indels indicate S. gigantea is the maternal genome donor. However, we did not recover a S. gigantea nrDNA sequence type. Taken together, these data reveal both a single origin and a complex pattern of reticulation that is consistent not only with the hypothesized allo- hexaploid nature of this species, but also with chloroplast capture of cpDNA from an unexpected source through introgression. Keywords— cpDNA , introgression , nrDNA , reticulate evolution , Solidago houghtonii . Interspecific hybridization and polyploidization have con- origin of Iris nelsonii Rand., a stabilized hybrid from southern tributed greatly to the diversification and speciation of plants Louisiana that displayed morphological and chromosomal ( Grant 1981 ; Arnold 1997 ; Rieseberg 1997 ; Soltis and Soltis characteristics of three sympatric Iris L. species. The use of 2000 ). Several lines of evidence have been used to elucidate allozyme data confirmed that I. nelsonii possessed a combi- the origins and evolutionary history of polyploid plant taxa. nation of genetic markers indicating the involvement of all Early studies focused on morphological, cytogenetic, and three sympatric taxa as parental donors. However, in none allozyme data. More recently, DNA sequence data obtained of these cases were the naturally occurring triple hybrids from both the uniparentally inherited chloroplast genome and reported to be hexaploid. Kaplan and Fehrer (2007) used the biparentally inherited nuclear genome have been used to the ITS region and cpDNA sequence data to reveal the pres- clarify the phylogenetic affinities of several polyploid species ence of three genomes in a persistent, but sterile, naturally (reviewed in Arnold 1997 ; Rieseberg 1997 ). Molecular phylo- occurring hexaploid Potamogeton L. clone. Here we investi- genetic analyses of allopolyploid plant taxa have shown that gate the origin and evolution of the naturally occurring fer- many have formed multiple times from independent hybrid- tile hexaploid, Solidago houghtonii Torrey & A. Gray ex Gray Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.151 on: Tue, 28 Sep 2021 22:00:33 ization events ( Soltis and Soltis 1993 , 1999 ), complex relation- (Asteraceae: Astereae: Solidagininae), a member of a hybrid- ships involving multiple unexpected genome donors ( Cronn ization “hotspot” family ( Ellstrand et al. 1996 ). et al. 2003 ; Mason-Gamer 2004 ), and cpDNA introgression Solidago L. is characterized by a perennial habit, outcross- into polyploid lineages ( Wendel 1989 ; Dorado et al. 1992 ; ing breeding system, and clonal reproduction, all character- Liston and Kadereit 1995 ; Cronn et al. 2003 ). istics identified by Ellstrand et al. (1996) as advantageous Kaplan and Fehrer (2007) point out that the majority of lit- to the formation and stabilization of hybrid taxa. The genus erature on plant hybridization is based on binary hybrids and includes about 100 North American species, with the great- that most of those are focused on the origin of allotetraploids. est number of these occurring in eastern North America In contrast, the literature contains few examples of studies ( Semple and Cook 2006 ). Additionally, there are six to ten using molecular tools to reveal the origin of recently formed species that are native to Eurasia, eight in Mexico, and four natural hybrids between three (or more) species. According in South America. Although there are no distinct morpho- to these authors, most of the literature on triple hybrids 1) logical synapomorphies that define Solidago ( Schilling et al. is based on morphology and presented in the context of 2008 ), most species are easily recognized as “goldenrods” local floras, 2) reports on the experimental production of tri- by their numerous, small heads of yellow florets. However, ple hybrids, or 3) is focused on ancient hybridization events morphological complexity within the genus often makes spe- involving three or more species and that the majority of these cies identification difficult. Clear delineation of species is fur- studies are based on the grasses and grain crops. ther complicated, not only by the occurrence of interspecific Recent naturally occurring hybrids between three of more hybrids, but also because many species are polytopic, and species have been reported for Aesculus L. ( dePamphilis and several species have multiple cytotypes including both dip- Wyatt 1990 ) and Quercus L. ( Dodd and Afzal-Rafii 2004 ). loids and polyploids (See Semple and Cook 2006 for poly- Using allozyme and AFLP markers, respectively, each study topic species and ploidy numbers). Gleason and Cronquist found that, in populations devoid of morphologically iden- (1991) divided the genus into groups based on three indepen- tifiable hybrids, genes from at least two species had been dent characters: (1) the structure of the underground parts introgressed into a third. Arnold et al. (1990) investigated the which vary from a short, stout caudex producing clumps of 209 210 SYSTEMATIC BOTANY [Volume 36 stems to a more slender and elongate rhizome with scattered stems; (2) the shape and distribution of the leaves which vary from basally disposed to chiefly cauline; and (3) the inflo- rescence type. In a few species the inflorescence is axillary, but most have a terminal inflorescence that can broadly be described as either paniculiform, racemiform, or corymbi- form. Based primarily on morphology, the genus has been divided into differing numbers of sections and subsections. Nesom (1993) presented a taxonomic overview in which he recognized two sections, section Solidago L. with four subsec- tions and section Unilaterales G. Don with seven subsections. Nesom also segregated two taxa that had previously been treated within Solidago : Oligoneuron Small and Oreochrysum Rydberg. According to this view, the genus Oligoneuron includes six species that are distinguished morphologically from the other members of Solidago by their corymboid (flat- Fig. 1. Geographic distribution of Solidago houghtonii . Dots indicate approximate location of known populations based on USFWS (1997) and topped) inflorescence, punctate leaves, broader phyllaries, COSEWIC (2005) . Boxes indicate four hypothesized entities for Solidago and larger achenes. Additionally, Nesom cites a “paucity houghtonii ( USFWS 1997 ). Entity 1: S. ptarmicoides (2 n = 18) × S. riddellii of natural hybridization” between taxa of Oligoneuron and (2 n = 18); entity 2: S. ptarmicoides (2 n = 18) × S. ohioensis (2 n = 18); entity 3: those of Solidago as further support for the segregation of S. ptarmicoides (2 n = 18) × S. uliginosa (2 n = 36); entity 4: S. ptarmicoides (2 n = 18) × S. uliginosa (2 n = 18). Collection localities for samples included in this Oligoneuron . Most recently, Semple and Cook (2006) have pre- study are indicated by arrows and referenced by their accession number. sented a taxonomic treatment of Solidago in which they rec- Figure modified from Guire and Voss (1963) . ognized section Solidago with eleven subsections and section Ptarmicoidei (House) Semple and Gandi. They placed the six corymboid taxa, recognized by Nesom (1993) as Oligoneuron , (Torrey & A. Gray) B. Boivin. He, as well as Mitchell and within Solidago section Ptarmicoidei . This is significant because Sheviak (1981) , further proposed that the New York plants were our species of interest, Solidago houghtonii, is one of the corym- of independent
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