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Research Evolution of L-DOPA 4,5-dioxygenase activity allows for recurrent specialisation to betalain pigmentation in Caryophyllales Hester Sheehan1* , Tao Feng1,2* , Nathanael Walker-Hale1* , Samuel Lopez-Nieves1 , Boas Pucker1,3 , Rui Guo1,2,4 , Won C. Yim5 , Roshani Badgami1 , Alfonso Timoneda1 , Lijun Zhao6 , Helene Tiley7 , Dario Copetti8,9,10 , Michael J. Sanderson11 , John C. Cushman5 , Michael J. Moore7 , Stephen A. Smith6 and Samuel F. Brockington1 1Department of Plant Sciences, University of Cambridge, Tennis Court Road, Cambridge, CB2 3EA, UK; 2CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; 3CeBiTec & Faculty of Biology, Bielefeld University, Universitaetsstrasse, Bielefeld 33615, Germany; 4College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China; 5Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV 89577, USA; 6Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA; 7Department of Biology, Oberlin College, Science Center K111, Oberlin, OH 44074, USA; 8Arizona Genomics Institute, School of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA; 9Molecular Plant Breeding, Institute of Agricultural Sciences, ETH Zurich, Universitaetstrasse 2, 8092, Zurich, Switzerland; 10Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland; 11Department of Ecology and Evolutionary Biology, University of Arizona, 1041 E. Lowell St, Tucson, AZ 85721, USA Summary Author for correspondence: The evolution of L-DOPA 4,5-dioxygenase activity, encoded by the gene DODA, was a key Samuel F. Brockington step in the origin of betalain biosynthesis in Caryophyllales. We previously proposed that L- Tel: +44 (0)1223 336268 DOPA 4,5-dioxygenase activity evolved via a single Caryophyllales-specific neofunctionalisa- Email: [email protected] tion event within the DODA gene lineage. However, this neofunctionalisation event has not Received: 30 May 2019 been confirmed and the DODA gene lineage exhibits numerous gene duplication events, Accepted: 22 July 2019 whose evolutionary significance is unclear. To address this, we functionally characterised 23 distinct DODA proteins for L-DOPA 4,5- New Phytologist (2019) dioxygenase activity, from four betalain-pigmented and five anthocyanin-pigmented species, doi: 10.1111/nph.16089 representing key evolutionary transitions across Caryophyllales. By mapping these functional data to an updated DODA phylogeny, we then explored the evolution of L-DOPA 4,5-dioxy- Key words: anthocyanins, betalains, genase activity. Caryophyllales, convergent evolution, gene We find that low L-DOPA 4,5-dioxygenase activity is distributed across the DODA gene lin- duplication, L-DOPA 4, 5-dioxygenase eage. In this context, repeated gene duplication events within the DODA gene lineage give rise (DODA), metabolic operon, plant pigments, to polyphyletic occurrences of elevated L-DOPA 4,5-dioxygenase activity, accompanied by specialised metabolism. convergent shifts in key functional residues and distinct genomic patterns of micro-synteny. In the context of an updated organismal phylogeny and newly inferred pigment reconstruc- tions, we argue that repeated convergent acquisition of elevated L-DOPA 4,5-dioxygenase activity is consistent with recurrent specialisation to betalain synthesis in Caryophyllales. have evolved to replace anthocyanins, which are otherwise ubiq- Introduction uitous across flowering plants (Bischoff, 1876; Clement & As sessile organisms, plants have exploited metabolic systems to Mabry, 1996). Betalains are also present in the fungal lineage produce a plethora of diverse specialised metabolites (Weng, Basidiomycota (Musso, 1979) and the bacterial species 2014). Specialised metabolites are critical for survival in particu- Gluconacetobacter diazotrophicus (Contreras-Llano et al., 2019). lar ecological niches and are often taxonomically restricted The phylogenetic distribution of betalain pigmentation within (Weng, 2014). In flowering plants, one remarkable example of a Caryophyllales is complex (Brockington et al., 2011). In betalain- taxonomically restricted specialised metabolite occurs in the producing families within the core Caryophyllales, anthocyanins angiosperm order Caryophyllales (Brockington et al., 2011; have not been found (Bate-Smith, 1962; Clement & Mabry, Timoneda et al., 2019). Here, tyrosine-derived betalain pigments 1996), although earlier substrates and associated enzymes in the flavonoid pathway have been detected (Shimada et al., 2004, *These authors contributed equally to this work. 2005; Polturak et al., 2018). However, anthocyanins have been Ó 2019 The Authors New Phytologist (2019) 1 New Phytologist Ó 2019 New Phytologist Trust www.newphytologist.com This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. New 2 Research Phytologist reported in six core Caryophyllales families, namely Caryophyl- biosynthesis involves conversion of L-3,4-dihydroxyphenylalanine laceae, Molluginaceae, Kewaceae, Limeaceae, Macarthuriaceae (L-DOPA) to betalamic acid, the central chromophore of betalain and Simmondsiaceae (Clement & Mabry, 1996; Thulin et al., pigments. L-DOPA 4,5-dioxygenase is encoded by the gene 2016). In these six anthocyanic lineages, betalains have not been DODA, a member of the LigB gene family (Christinet et al., detected, indicating that anthocyanins and betalains are mutually 2004). Within Caryophyllales, a gene duplication in the LigB/ exclusive (Stafford, 1994; Clement & Mabry, 1996). The six DODA gene lineage gave rise to the DODAa and DODAb anthocyanic lineages are intercalated with betalain-pigmented clades, with L-DOPA 4,5-dioxygenase activity previously inferred lineages resulting in a homoplastic distribution of these two pig- to have evolved at the base of the DODAa lineage (Brockington ments (Brockington et al., 2011). The distribution of antho- et al., 2015). On the basis of this Caryophyllales-specific cyanin and betalain-pigmented lineages is consistent with DODAa/DODAb duplication, and subsequent losses of multiple origins of betalain pigmentation, a single origin of beta- DODAa loci in anthocyanic lineages, we previously argued for a lain pigmentation with multiple reversals to anthocyanin, or a single origin of betalain pigmentation, with multiple reversals to combination of these scenarios (Brockington et al., 2011). anthocyanin pigmentation (Brockington et al., 2015). In contrast to the anthocyanin pathway, the betalain biosyn- However, evolutionary patterns within the DODAa lineage thetic pathway is relatively simple, involving as few as four enzy- are complex (Brockington et al., 2015). In addition to the matic steps to proceed from tyrosine to stable betalain pigments: DODAa/DODAb duplication, there have been at least nine yellow betaxanthins and violet betacyanins (Fig. 1). The core duplications in the DODAa lineage resulting in all betalain-pig- genes encoding betalain synthesis enzymes have been elucidated, mented lineages of Caryophyllales containing at least three primarily through heterologous assays in Saccharomyces cerevisiae DODA genes – at least one homologue from the DODAb lineage and Nicotiana benthamiana, which has emerged as an essential and at least two paralogues from the DODAa lineage, with Beta tool for betalain research in planta (Polturak et al., 2016; vulgaris containing five copies of DODAa.InB. vulgaris, only Timoneda et al., 2018). The key enzymatic step in betalain two DODAa paralogues have been studied (Sasaki et al., 2009; OOH OOH H H NH 2 NH2 Tyrosine hydroxylase HO OH CYP76AD1/5/6/15 OH Tyrosine L-DOPA L-DOPA 4,5-dioxygenase L-DOPA oxidase DODA CYP76AD1/3 O O R H OH H H Spontaneous N H HO NH2 Spontaneous O O OH N HO Amino or OH H O OH amine group Betalamic acid cyclo-DOPA OH OH HO R H O O H HO N+ OH O O O O cDOPA glucosyltransferase O + N+ HO N O HO cDOPA5GT Glucosyltransferase HN OH O OH N Betanidin 5GT/6GT O OH OH H OH HO O N O H Betanidin OH O OH Betaxanthin Betacyanin H N H O O HO OH OH Spontaneous HO OH cDOPA 5-O-glucoside Fig. 1 The betalain biosynthetic pathway. A schematic showing the enzymatic and spontaneous reactions that form the specialised metabolites, betalains. The focus of this study is L-DOPA 4,5-dioxygenase (DODA; highlighted in red) which catalyses the formation of betalamic acid, the core chromophore of betalain pigments, from L-3,4-dihydroxyphenylalanine (L-DOPA). This figure was adapted from Timoneda et al. (2019). New Phytologist (2019) Ó 2019 The Authors www.newphytologist.com New Phytologist Ó 2019 New Phytologist Trust New Phytologist Research 3 Gandıa-Herrero & Garcıa-Carmona, 2012; Hatlestad et al., Pollichia campestris Aiton, Corrigiola litoralis L., Spergula arvensis 2012; Chung et al., 2015; Bean et al., 2018), with one paralogue, L. and Simmondsia chinensis Link C.K. were grown at the Cam- BvDODA1 (hereafter termed BvDODAa1), found to exhibit bridge University Botanic Garden under natural conditions. high levels of L-DOPA 4,5-dioxygenase activity and the other Fresh tissue of Polycarpon tetraphyllum (L.) L. was collected in paralogue, BvDODA2 (hereafter termed BvDODAa2), exhibit- Florida (Lake Wauburg Recreation Area, Alachua County, FL, ing no or only marginal L-DOPA 4,5-dioxygenase
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  • Baja California, Mexico, and a Vegetation Map of Colonet Mesa Alan B

    Baja California, Mexico, and a Vegetation Map of Colonet Mesa Alan B

    Aliso: A Journal of Systematic and Evolutionary Botany Volume 29 | Issue 1 Article 4 2011 Plants of the Colonet Region, Baja California, Mexico, and a Vegetation Map of Colonet Mesa Alan B. Harper Terra Peninsular, Coronado, California Sula Vanderplank Rancho Santa Ana Botanic Garden, Claremont, California Mark Dodero Recon Environmental Inc., San Diego, California Sergio Mata Terra Peninsular, Coronado, California Jorge Ochoa Long Beach City College, Long Beach, California Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Biodiversity Commons, Botany Commons, and the Ecology and Evolutionary Biology Commons Recommended Citation Harper, Alan B.; Vanderplank, Sula; Dodero, Mark; Mata, Sergio; and Ochoa, Jorge (2011) "Plants of the Colonet Region, Baja California, Mexico, and a Vegetation Map of Colonet Mesa," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 29: Iss. 1, Article 4. Available at: http://scholarship.claremont.edu/aliso/vol29/iss1/4 Aliso, 29(1), pp. 25–42 ’ 2011, Rancho Santa Ana Botanic Garden PLANTS OF THE COLONET REGION, BAJA CALIFORNIA, MEXICO, AND A VEGETATION MAPOF COLONET MESA ALAN B. HARPER,1 SULA VANDERPLANK,2 MARK DODERO,3 SERGIO MATA,1 AND JORGE OCHOA4 1Terra Peninsular, A.C., PMB 189003, Suite 88, Coronado, California 92178, USA ([email protected]); 2Rancho Santa Ana Botanic Garden, 1500 North College Avenue, Claremont, California 91711, USA; 3Recon Environmental Inc., 1927 Fifth Avenue, San Diego, California 92101, USA; 4Long Beach City College, 1305 East Pacific Coast Highway, Long Beach, California 90806, USA ABSTRACT The Colonet region is located at the southern end of the California Floristic Province, in an area known to have the highest plant diversity in Baja California.