Genetic architecture of floral traits in bee- and hummingbird-pollinated sister species of Aquilegia (columbine)

Interactions with animal pollinators have helped shape the stunning diversity of flower morphologies across the angiosperms. A common evolutionary consequence of these interactions is that some flowers have converged on suites of traits, or pollination syndromes, that attract and reward specific pollinator groups. Determining the genetic basis of these floral pollination syndromes can help us understand the processes that contributed to the diversification of the angiosperms. Here, we characterize the genetic architecture of a bee-to-hummingbird pollination shift in Aquilegia (columbine) using QTL mapping of 17 floral traits encompassing color, nectar composition, and organ morphology. In this system, we find that the genetic architectures underlying differences in floral color are quite complex, and we identify several likely candidate genes involved in anthocyanin and carotenoid floral pigmentation. Most morphological and nectar traits also have complex genetic underpinnings; however, one of the key floral morphological phenotypes, nectar spur curvature, is shaped by a single locus of large effect.

[1]  E. Kramer,et al.  POPOVICH, encoding a C2H2 zinc-finger transcription factor, plays a central role in the development of a key innovation, floral nectar spurs, in Aquilegia , 2020, Proceedings of the National Academy of Sciences.

[2]  Z. Fang,et al.  Insertion of a CACTA-like transposable element disrupts the function of the BoCCD4 gene in yellow-petal Chinese kale , 2019, Molecular Breeding.

[3]  L. Hileman,et al.  Nectary size is a pollination syndrome trait in Penstemon , 2019, The New phytologist.

[4]  Richard D. Hayes,et al.  The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history , 2018, eLife.

[5]  E. Kramer,et al.  Homologs of the STYLISH gene family control nectary development in Aquilegia. , 2018, The New phytologist.

[6]  A. Ohmiya,et al.  Regulation of Carotenoid Pigmentation in Corollas of Petunia , 2018, Plant Molecular Biology Reporter.

[7]  D. Lewis,et al.  Insights into carotenoid accumulation using VIGS to block different steps of carotenoid biosynthesis in petals of California poppy , 2018, Plant Cell Reports.

[8]  R. Roy,et al.  Review: Nectar biology: From molecules to ecosystems. , 2017, Plant science : an international journal of experimental plant biology.

[9]  R. Gegear,et al.  "Hummingbird" floral traits interact synergistically to discourage visitation by bumble bee foragers. , 2017, Ecology.

[10]  Miao Wu,et al.  Characterization of OfWRKY3, a transcription factor that positively regulates the carotenoid cleavage dioxygenase gene OfCCD4 in Osmanthus fragrans , 2016, Plant Molecular Biology.

[11]  Stacey D. Smith,et al.  How to make a red flower: the combinatorial effect of pigments , 2016, AoB PLANTS.

[12]  Yao-wu Yuan,et al.  Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species , 2016, Proceedings of the National Academy of Sciences.

[13]  Emily M. Strait,et al.  The arabidopsis information resource: Making and mining the “gold standard” annotated reference plant genome , 2015, Genesis.

[14]  L. Levin,et al.  Biodiversity on the Rocks: Macrofauna Inhabiting Authigenic Carbonate at Costa Rica Methane Seeps , 2015, PloS one.

[15]  D. Ware,et al.  Metabolomic Profiling of the Nectars of Aquilegia pubescens and A. Canadensis , 2015, PloS one.

[16]  L. Yant,et al.  Molecular basis for three-dimensional elaboration of the Aquilegia petal spur , 2015, Proceedings of the Royal Society B: Biological Sciences.

[17]  C. Kuhlemeier,et al.  The genetics of reproductive organ morphology in two Petunia species with contrasting pollination syndromes , 2015, Planta.

[18]  M. Rausher,et al.  Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[19]  M. Rausher,et al.  PREDICTABILITY AND IRREVERSIBILITY OF GENETIC CHANGES ASSOCIATED WITH FLOWER COLOR EVOLUTION IN PENSTEMON BARBATUS , 2014, Evolution; international journal of organic evolution.

[20]  W. Frommer,et al.  Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9 , 2014, Nature.

[21]  S. Knapp,et al.  Genetic architecture of floral traits in Iris hexagona and Iris fulva. , 2013, The Journal of heredity.

[22]  E. Vranová,et al.  Characterization of the GGPP synthase gene family in Arabidopsis thaliana , 2013, Plant Molecular Biology.

[23]  L. Rieseberg,et al.  The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae) , 2013, Heredity.

[24]  R. Viola,et al.  Spatiotemporal reconstruction of the Aquilegia rapid radiation through next-generation sequencing of rapidly evolving cpDNA regions. , 2013, The New phytologist.

[25]  A. Cardona,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[26]  Thomas L. Madden,et al.  Domain enhanced lookup time accelerated BLAST , 2012, Biology Direct.

[27]  M. Rockman THE QTN PROGRAM AND THE ALLELES THAT MATTER FOR EVOLUTION: ALL THAT'S GOLD DOES NOT GLITTER , 2012, Evolution; international journal of organic evolution.

[28]  R. Aebersold,et al.  Mapping the interaction of Snf1 with TORC1 in Saccharomyces cerevisiae , 2011, Molecular systems biology.

[29]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[30]  M. Rausher,et al.  Gene loss and parallel evolution contribute to species difference in flower color. , 2011, Molecular biology and evolution.

[31]  C. Kuhlemeier,et al.  The genetic architecture of natural variation in flower morphology. , 2011, Current opinion in plant biology.

[32]  M. Rausher,et al.  Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii , 2011, Nature.

[33]  P. Christou,et al.  The regulation of carotenoid pigmentation in flowers. , 2010, Archives of biochemistry and biophysics.

[34]  W. Frommer,et al.  Sugar transporters for intercellular exchange and nutrition of pathogens , 2010, Nature.

[35]  Y. Ozeki,et al.  A Novel Glucosylation Reaction on Anthocyanins Catalyzed by Acyl-Glucose–Dependent Glucosyltransferase in the Petals of Carnation and Delphinium[C][W] , 2010, Plant Cell.

[36]  T. Banchoff,et al.  Differential Geometry of Curves and Surfaces , 2010 .

[37]  A. Ohmiya Carotenoid cleavage dioxygenases and their apocarotenoid products in plants , 2009 .

[38]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[39]  M. V. Price,et al.  A global test of the pollination syndrome hypothesis. , 2009, Annals of botany.

[40]  U. Stenzel,et al.  PatMaN: rapid alignment of short sequences to large databases , 2008, Bioinform..

[41]  Yoshikazu Tanaka,et al.  Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. , 2008, The Plant journal : for cell and molecular biology.

[42]  Q. Cronk,et al.  Bird-pollinated flowers in an evolutionary and molecular context. , 2008, Journal of experimental botany.

[43]  J. Thomson,et al.  Constrained lability in floral evolution: counting convergent origins of hummingbird pollination in Penstemon and Keckiella. , 2007, The New phytologist.

[44]  S. Tanksley,et al.  Changes in Regulation of a Transcription Factor Lead to Autogamy in Cultivated Tomatoes , 2007, Science.

[45]  S. Wessler,et al.  QTL ANALYSIS OF FLORAL TRAITS IN LOUISIANA IRIS HYBRIDS , 2007, Evolution; international journal of organic evolution.

[46]  S. Hodges,et al.  Pollinator shifts drive increasingly long nectar spurs in columbine flowers , 2007, Nature.

[47]  Toshio Yamamoto,et al.  Marker-assisted selection and evaluation of the QTL for stigma exsertion under japonica rice genetic background , 2007, Theoretical and Applied Genetics.

[48]  R. Pérez,et al.  Intra-plant variation in nectar sugar composition in two Aquilegia species (Ranunculaceae): contrasting patterns under field and glasshouse conditions. , 2006, Annals of botany.

[49]  H. Bouwmeester,et al.  Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways , 2006, Planta.

[50]  C. Ritland,et al.  THE GENETIC BASIS OF FLORAL TRAITS ASSOCIATED WITH MATING SYSTEM EVOLUTION IN LEPTOSIPHON (POLEMONIACEAE): AN ANALYSIS OF QUANTITATIVE TRAIT LOCI , 2006, Evolution; international journal of organic evolution.

[51]  C. Kuhlemeier,et al.  The genetic dissection of floral pollination syndromes. , 2006, Current opinion in plant biology.

[52]  J. Micol,et al.  Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture , 2005, Evolution & development.

[53]  Christopher R. Herlihy,et al.  Evolution of self-fertilization at geographical range margins? A comparison of demographic, floral, and mating system variables in central vs. peripheral populations of Aquilegia canadensis (Ranunculaceae). , 2005, American journal of botany.

[54]  S. Via,et al.  Back to the future: genetic correlations, adaptation and speciation , 2005, Genetica.

[55]  Michele R. Dudash,et al.  Pollination Syndromes and Floral Specialization , 2004 .

[56]  C. Kuhlemeier,et al.  Dissection of Floral Pollination Syndromes in Petunia , 2004, Genetics.

[57]  L. Carretero-Paulet,et al.  Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. , 2004, The Plant journal : for cell and molecular biology.

[58]  S. Hodges,et al.  Verne Grant and evolutionary studies of Aquilegia , 2003 .

[59]  D. Schemske,et al.  Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers , 2003, Nature.

[60]  D. Lewis,et al.  Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase , 2003, Euphytica.

[61]  Hao Wu,et al.  R/qtl: QTL Mapping in Experimental Crosses , 2003, Bioinform..

[62]  R. Stracke,et al.  The R2R3-MYB gene family in Arabidopsis thaliana. , 2001, Current opinion in plant biology.

[63]  D. Garvin,et al.  A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). , 2001, The Plant journal : for cell and molecular biology.

[64]  C. Eckert,et al.  Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis (Ranunculaceae) , 1999, Heredity.

[65]  D. Grimaldi The Co-Radiations of Pollinating Insects and Angiosperms in the Cretaceous , 1999 .

[66]  M. Arnold,et al.  Spurring plant diversification: are floral nectar spurs a key innovation? , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  D. Schemske,et al.  Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus) , 1995, Nature.

[68]  R. J. Taylor Floral anthocyanins of Aquilegia and their relationship to distribution and pollination biology of the species , 1984 .

[69]  A. Gerats,et al.  Genetic control of the conversion of dihydroflavonols into flavonols and anthocyanins in flowers of Petunia hybrida , 1982, Planta.

[70]  H. G. Baker,et al.  On the calculation of sugar concentration in flower nectar , 1979, Oecologia.

[71]  H. G. Baker Sugar concentrations in nectar from hummingbird flowers , 1975 .

[72]  V. Grant,et al.  POLLINATION SYSTEMS AS ISOLATING MECHANISMS IN ANGIOSPERMS , 1949, Evolution; international journal of organic evolution.

[73]  W. T. THISELTON DYER,et al.  The Effects of Cross- and Self-Fertilisation in the Vegetable Kingdom , 1877, Nature.

[74]  T. Nakayama,et al.  Achievements and perspectives in biochemistry concerning anthocyanin modification for blue flower coloration. , 2015, Plant & cell physiology.

[75]  M. Nakayama,et al.  Contribution made by the carotenoid cleavage dioxygenase 4 gene to yellow colour fade in azalea petals , 2015, Euphytica.

[76]  W. Prażmo Cytogenetic studies on the genus Aquilegia, III. Inheritance of the traits distinguishing different complex in the genus Aquilegia , 2015 .

[77]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[78]  C. Kuhlemeier,et al.  Color and scent: how single genes influence pollinator attraction. , 2012, Cold Spring Harbor symposia on quantitative biology.

[79]  W. Armbruster,et al.  Associations between floral specialization and species diversity: cause, effect, or correlation? , 2008, Evolutionary Ecology.

[80]  Claude-Alain H. Roten,et al.  Theoretical and practical advances in genome halving , 2004 .

[81]  William L. Crepet,et al.  Advanced (Constant) Insect Pollination Mechanisms: Pattern of Evolution and Implications Vis-a-Vis Angiosperm Diversity , 1984 .

[82]  L. W. Macior Pollination ecology of vernal angiosperms , 1978 .

[83]  J. Schulte,et al.  Spurring plant diversification : Are floral nectar spurs a key innovation ? , 2022 .