Abstract
CRABS CLAW (CRC), a member of YABBY transcription factor family, has been previously reported to be principally involved in carpel development across angiosperms, and nectary development in core eudicots. Most of the studies suggest that CRC exists as a single copy gene, except in the Solanaceae where CRC occurs as paralogous pairs—CRCa–CRCb in Solanum lycopersicum, and CRC1–CRC2 in Petunia hybrida. In spite of their crucial role in carpel and nectary development, there is no information about the evolutionary history of the CRC paralogy in Solanaceae and whether the paralogy extends beyond Solanaceae. We analyzed homologues of CRC across angiosperms including genome sequence of fourteen species of Solanaceae available at Sol Genomics Network database, Phytozome and NCBI, to address the questions. Our phylogenetic reconstruction across angiosperms combined with comparative genomic, microsynteny and genome-fractionation analyses across the Solanaceae genomes revealed that (1) the CRCa–CRCb lineage is represented by a single copy in other flowering plants; (2) putative homologues of CRCa and CRCb are present in all the Solanaceae genomes studied; (3) the CRCa–CRCb paralogy in Solanaceae is associated with a large segmental duplication within Solanaceae (perhaps in its common ancestor), and (4) the duplicated segments have undergone different degrees of retention and loss of genes. Also, the CRC gene lineage expanded in Solanaceae following Solanaceae-α hexaploidy event and that two CRC duplicate copies were subsequently retained during the course of evolution. Besides the first detailed description of CRC evolution in Solanaceae, the study identifies potential candidate genes for future functional investigations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bartholmes C, Hidalgo O, Gleissberg S (2012) Evolution of the yabby gene family with emphasis on the basal eudicot Eschscholzia californica (Papaveraceae). Plant Biol 14:11–23. https://doi.org/10.1111/j.1438-8677.2011.00486.x
Bernardello G (2007) A systematic survey of floral nectaries. In: Nicolson SW, Pacini E, Nepi M (eds) Nectaries and nectar. Springer, Dordrecht, pp 19–128
Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant–microbe biology research. Mol Plant Microbe Interact 25:1523–1530. https://doi.org/10.1094/MPMI-06-12-0148-TA
Bombarely A, Moser M, Amrad A, Bao M, Bapaume L, Barry CS, Bliek M, Boersma MR, Borghi L, Bruggmann R, Bucher M (2016) Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat Plants. https://doi.org/10.1038/nplants.2016.74
Bowman JL, Smyth DR (1999) Crabs claw, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396
Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Mol Phylogenet Evol 33:75–90. https://doi.org/10.1016/j.ympev.2004.05.002
Ezura K, Ji-Seong K, Mori K, Suzuki Y, Kuhara S, Ariizumi T, Ezura H (2017) Genome-wide identification of pistil-specific genes expressed during fruit set initiation in tomato (Solanum lycopersicum). PLoS One 12:e0180003. https://doi.org/10.1371/journal.pone.0180003
Fourquin C, Primo A, Martínez-Fernández I, Huet-Trujillo E, Ferrándiz C (2014) The CRC orthologue from Pisum sativum shows conserved functions in carpel morphogenesis and vascular development. Ann Bot 114:1535–1544. https://doi.org/10.1093/aob/mcu129
Frary A, Doganlar S, Frary A (2016) Synteny among Solanaceae genomes. In: Giovannoni J, Bouzayen M, Zouine M, Causse M (eds) The tomato genome. compendium of plant genomes. Springer, Berlin, pp 217–243
Huang Z, Van Houten J, Gonzalez G, Xiao H, van der Knaap E (2013) Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Mol Genet Genomics 288:111–129. https://doi.org/10.1007/s00438-013-0733-0
Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Vezzi A (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463. https://doi.org/10.1038/nature06148
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97. https://doi.org/10.1038/nature09916
Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Mol Genet Genom 240:159–169. https://doi.org/10.1007/BF00277053
Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022. https://doi.org/10.1093/jxb/erf068
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lee JY, Baum SF, Alvarez J, Patel A, Chitwood DH, Bowman JL (2005a) Activation of crabs claw in the nectaries and carpels of Arabidopsis. Plant Cell 17:25–36. https://doi.org/10.1105/tpc.104.026666
Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005b) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032. http://dev.biologists.org/cgi/content/full/132/22/5021/DC1
Morel P, Heijmans K, Ament K, Chopy M, Trehin C, Chambrier P, Bento SR, Bimbo A, Vandenbussche M (2018) The floral C-lineage genes trigger nectary development in Petunia and Arabidopsis. Plant Cell 30:2020–2037. https://doi.org/10.1105/tpc.18.00425
Nakayama H, Yamaguchi T, Tsukaya H (2010) Expression patterns of AaDL, a crabs claw ortholog in Asparagus asparagoides (Asparagaceae), demonstrate a stepwise evolution of CRC/DL subfamily of YABBY genes. Am J Bot 97:591–600. https://doi.org/10.3732/ajb.0900378
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181. https://doi.org/10.1002/tax.574010
Orashakova S, Lange M, Lange S, Wege S, Becker A (2009) The crabs claw ortholog from California poppy (Eschscholzia californica, Papaveraceae), EcCRC, is involved in floral meristem termination, gynoecium differentiation and ovule initiation. Plant J 58:682–693. https://doi.org/10.1111/j.1365-313X.2009.03807.x
Park M, Jo S, Kwon JK, Park J, Ahn JH, Kim S, Lee YH, Yang TJ, Hur CG, Kang BC, Kim BD (2011) Comparative analysis of pepper and tomato reveals euchromatin expansion of pepper genome caused by differential accumulation of Ty3/Gypsy-like elements. BMC Genom 12:85. https://doi.org/10.1186/1471-2164-12-85
Peters SA, Bargsten JW, Szinay D, van de Belt J, Visser RG, Bai Y, de Jong H (2012) Structural homology in the Solanaceae: analysis of genomic regions in support of synteny studies in tomato, potato and pepper. Plant J 71:602–614. https://doi.org/10.1111/j.1365-313X.2012.05012.x
Pfannebecker KC, Lange M, Rupp O, Becker A (2016) An evolutionary framework for carpel developmental control genes. Mol Biol Evol 34:330–348. https://doi.org/10.1093/molbev/msw229
Pfannebecker KC, Lange M, Rupp O, Becker A (2017) Seed plant-specific gene lineages involved in carpel development. Mol Biol Evol 34:925–942. https://doi.org/10.1093/molbev/msw297
Singh S, Das S, Geeta R (2018) A segmental duplication in the common ancestor of Brassicaceae is responsible for the origin of the paralogs KCS6-KCS5, which are not shared with other angiosperms. Mol Phylogenet Evol 126:331–345. https://doi.org/10.1016/j.ympev.2018.04.018
Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7:S10. https://doi.org/10.1186/gb-2006-7-s1-s10
Stamatakis A, Hoover P, Rougemont J, Renner S (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771. https://doi.org/10.1080/10635150802429642
Sun W, Huang W, Li Z, Lv H, Huang H, Wang Y (2013) Characterization of a Crabs Claw gene in basal eudicot species Epimedium sagittatum (Berberidaceae). Int J Mol Sci 14:119–1131. https://doi.org/10.3390/ijms14011119
Tang H, Woodhouse MR, Cheng F, Schnable JC, Pedersen BS, Conant G, Wang X, Freeling M, Pires JC (2012) Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 190:1563–1574. https://doi.org/10.1534/genetics.111.137349
The Plant List (2013) Version 1.1. Published on the Internet. http://www.theplantlist.org
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635. https://doi.org/10.1038/nature11119
Vanneste K, Maere S, Van de Peer Y (2014) Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos Trans R Soc B Biol Sci 369:20130353. https://doi.org/10.1098/rstb.2013.0353
Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, Maere S, Van de Peer Y, Geuten K (2012) Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol Biol Evol 29:3793–3806. https://doi.org/10.1093/molbev/mss183
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035. https://doi.org/10.1038/ng.919
Yamada T, Yokota SY, Hirayama Y, Imaichi R, Kato M, Gasser CS (2011) Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. Plant J 67:26–36. https://doi.org/10.1111/j.1365-313X.2011.04570.x
Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The Yabby gene drooping leaf regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509. https://doi.org/10.1105/tpc.018044
Yang Z, Gong Q, Wang L, Jin Y, Xi J, Li Z, Qin W, Yang Z, Lu L, Chen Q, Li F (2018) Genome-wide study of YABBY genes in upland cotton and their expression patterns under different stresses. Front Genet 9:33. https://doi.org/10.3389/fgene.2018.00033
Funding
This work was supported by Research and Development grant, Grant no (RC/2015/9677) to RT is gratefully acknowledged. BP is thankful to the Council of Scientific and Industrial Research (CSIR) for the award of Junior and Senior Research Fellowships (09/045(1370)/2015-EMR-I).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Stefan Hohmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Phukela, B., Geeta, R., Das, S. et al. Ancestral segmental duplication in Solanaceae is responsible for the origin of CRCa–CRCb paralogues in the family. Mol Genet Genomics 295, 563–577 (2020). https://doi.org/10.1007/s00438-019-01641-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-019-01641-0