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The complete nucleotide sequence of the cassava (Manihot esculenta) chloroplast genome and the evolution of atpF in Malpighiales: RNA editing and multiple losses of a group II intron

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Abstract

The complete sequence of the chloroplast genome of cassava (Manihot esculenta, Euphorbiaceae) has been determined. The genome is 161,453 bp in length and includes a pair of inverted repeats (IR) of 26,954 bp. The genome includes 128 genes; 96 are single copy and 16 are duplicated in the IR. There are four rRNA genes and 30 distinct tRNAs, seven of which are duplicated in the IR. The infA gene is absent; expansion of IRb has duplicated 62 amino acids at the 3′ end of rps19 and a number of coding regions have large insertions or deletions, including insertions within the 23S rRNA gene. There are 17 intron-containing genes in cassava, 15 of which have a single intron while two (clpP, ycf3) have two introns. The usually conserved atpF group II intron is absent and this is the first report of its loss from land plant chloroplast genomes. The phylogenetic distribution of the atpF intron loss was determined by a PCR survey of 251 taxa representing 34 families of Malpighiales and 16 taxa from closely related rosids. The atpF intron is not only missing in cassava but also from closely related Euphorbiaceae and other Malpighiales, suggesting that there have been at least seven independent losses. In cassava and all other sequenced Malphigiales, atpF gene sequences showed a strong association between C-to-T substitutions at nucleotide position 92 and the loss of the intron, suggesting that recombination between an edited mRNA and the atpF gene may be a possible mechanism for the intron loss.

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Acknowledgments

Investigations reported in this article were supported in part by grants from the USDA (3611-21000-017-00D) and NIH (R01 GM 63879) to Henry Daniell. Research by Kenneth J. Wurdack and Robert K. Jansen was supported, in part, by NSF AToL grants EF 0431242 and DEB 0120709, respectively. The authors thank Kenneth Olsen, the Royal Botanic Gardens, Kew, and the herbaria cited for tissue or DNA samples.

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Authors and Affiliations

  1. Department Molecular Biology and Microbiology, College of Medicine, University of Central Florida, 4000 Central Florida Blvd, Biomolecular Science Bldg # 20, Room 336, Orlando, FL, 32816-2364, USA

    Henry Daniell, Anderson Kanagaraj & Seung-Bum Lee

  2. Department of Botany, Smithsonian Institution, NMNH MRC 166, P.O. Box 37012, Washington, DC, 20013-7012, USA

    Kenneth J. Wurdack

  3. Clemson University Genomics Institute, Biosystems Research Complex, Clemson University, 51 New Cherry Street, Clemson, SC, 29634, USA

    Christopher Saski

  4. Section of Integrative Biology and Institute of Cellular and Molecular Biology, University of Texas, Austin, TX, 78712, USA

    Robert K. Jansen

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  1. Henry Daniell
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Correspondence to Henry Daniell.

Additional information

Communicated by R. Hagemann.

Appendix

Appendix

Taxa and voucher information for 250 accessions (251 taxa) of Malpighiales and related families examined for atpF intron status. Taxa sequenced for atpF are followed by the GenBank accession number. Herbarium acronyms follow Index Herbariorum (http://sciweb.nybg.org/science2/IndexHerbariorum.asp).

Intron present

(i) Malpighiales

Achariaceae: Acharia tragodes Thunb., Cloete s.n. (BOL); Erythrospermum phytolaccoides Gardn., Chase 1277 (K); Hydnocarpus sp., Chase 1301 (K); Kiggelaria africana L., Chase 5607 (K). Balanopaceae: Balanops vieillardii Baill., Chase 1816 (K). Bonnetiaceae: Bonnetia sessilis Benth., Berry s.n. 25.7.98 (MO). Caryocaraceae: Anthodiscus amazonicus Gleason & A. C. Sm., van der Werff 13889 (MO); Caryocar glabrum Pers., Mori 22997 (NY). Clusiaceae s.l.: Mammea siamensis T. Anders., Chase 1216 (K); “Mesua” sp. (probably Kayea sp.), Coode 7884 (K); Montrouziera cauliflora Planch. & Triana, Lowry 5601 (MO); Pentaphalangium latissimum Lauterb., Chase 2100 (K); Rheedia macrophylla Planch. & Triana, Chase 1219 (K). Ctenolophonaceae: Ctenolophon englerianus Mildbr., McPherson 16911 (MO). Dichapetalaceae: Dichapetalum sp., Chase 624 (K?). Euphorbiaceae s.s.: Acalypha californica Benth., Levin 2192 (SD) GenBank EU293932; Adriana tomentosa (Thunb.) Gaudich. var. tomentosa, Cameron s.n. (US); Aleurites moluccana (L.) Willd., Wurdack s.n. (US); Amperea xiphoclada (Sieber ex Spreng.) Druce, Chase 1936 (K); Anthostema madagascariense Baill., Hoffmann 291 (K); Aparisthmium cordatum (A. Juss.) Baill., Bell et al. 93-60 (US); Astraea lobatum Klotzsch, Steinmann 2024 (RSA); Baloghia inophylla (G. Forst.) P. S. Green, Chase 3062 (K); Bernardia myricifolia (Scheele) S. Watson, McGill & Sundell 5459 (K); Bertya rosmarinifolia Planch., Chase 1938 (K); Beyeria leschenaultii (DC.) Baill., Chase 1939 (K); Blumeodendron sp., Chase 1252 (K); Calycopeplus casuarinoides L.S. Sm., Steinmann 1407 (RSA); Caperonia palustris (L.) A. St.-Hil., Wurdack D073 (US); Cavacoa aurea (Cavaco) J. Léonard, Luke & Robertson 1922 (US); Cephalomappa malloticarpa J.J. Sm., M. Chase 1256 (K); Chaetocarpus africanus Pax, Gabon, White 1319 (MO); Cladogynos orientalis Zipp., Chamchanroon 2010 (L); Claoxylon australe Baill. ex Müll. Arg., Chase 1937 (K); Clutia pulchella L., Chase 5876 (K); Cnesmone javanica Blume, Huq 10189 (US); Codiaeum variegatum (L.) Blume, Wurdack D033 (US), GenBank EU293933; Colliguaja integerrima Gillies & Hook., Landrum 8234 (MO); Conceveiba martiana Baill., Bell 93-176 (US); Croton alabamensis E.A. Sm. ex Chapm. var. alabamensis, Wurdack D008 (US), GenBankEU293934 Croton alabamensis E.A. Smith ex Chapman var. texensis Ginzbarg, Nesom 7850 (NY); Croton betulinus Vahl, Steinmann 2026 (RSA); Croton chilensis Müll. Arg., Wurdack D646 (US); Croton conduplicatus Kunth, Berry 5542 (MO); Croton cuneatus Klotzsch, Berry 7589 (PORT); Croton elliottii Chapm., Wurdack D455 (US); Croton flavens L., Steinmann 2015 (RSA); Croton guianensis Aubl., Berry 5535 (MO); Croton martinianus V.W.Steinm., Steinmann 606 (RSA); Croton nanus Gagnep., Pooma 4256 (BKF); Croton repens Schltdl., Steinmann 1062 (RSA); Croton setigerus Hook., Hughey s.n. (US); Croton socotranus Balf. f., Wurdack D644 (US); Croton speciosus Müll. Arg., Berry 7590 (MO); Croton suaveolens Torr., Devender 96-257 (RSA); Croton trinitatis Millsp., Berry 7586 (MO); Crotonogynopsis usambarica Pax, Tanzania, Polhill et al. 5129 (K); Dalechampia spathulata (Scheidw.) Baill., Wurdack D010 (US); Dichostemma glaucescens Pierre, Reitsma 1285 (NY); Ditaxis argothamnoides (Bertol. ex Spreng.) Radcl.-Sm. & Govaerts, Wurdack D105 (US); Ditrysinia fruticosa (Bartram) Govaerts & Frodin, Wurdack D149 (US); Ditta myricoides Griseb., Cedeño s.n. (US); Dodecastigma amazonicum Ducke, Mori 22811 (US); Endospermum moluccanum (Teijsm. & Binn.) Kurz, Chase 1258 (K); Enriquebeltrania crenatifolia (Miranda) Rzed., Cabrera 10768 (NY); Erythrococca sp., Cameroon, Cheek s.n. (K); Euphorbia epithymoides L., Chase 102 (NCU); Euphorbia mesembryanthemifolia Jacq., Wurdack D102 (US); Euphorbia pulcherrima Willd. ex Klotzsch cv. ‘Brilliant Diamonds’, Wurdack D084 (US); Excoecaria agallocha L., Motley & Cameron 2053 (NY); Excoecaria cochinchinensis Lour., Chase 1260 (K); Garcia nutans Vahl ex Rohr, Wurdack D051 (US); Gitara venezolana Pax & K. Hoffm., Bell et al. 94-312 (US); Gymnanthes lucida Sw., Wurdack D055 (US); Hippomane mancinella L., Wurdack D053 (US); Homalanthus populneus (Geiseler) Pax, Chase 1266 (K); Hura crepitans L., Wurdack D089 (US) GenBankEU293935; Jatropha gossypifolia L., Tayor 11763 (MO); Jatropha integerrima Jacq., Wurdack D047 (US); Joannesia princeps Vell., Chase 1262 (K); Klaineanthus gaboniae Pierre, White (ser. 2) 334 (MO); Koilodepas bantamense Hassk., Chase 1263 (K); Lasiocroton bahamensis Pax & K. Hoffm., Wurdack D058 (US); Leucocroton microphyllus (A. Rich.) Pax & K. Hoffm., HAJB 81915 (HAJB); Mabea sp., Bell et al. 94-30 (US); Macaranga grandifolia (Blanco) Merr., Wurdack D046 (US); Mallotus japonicus (L. f.) Müll. Arg., Wurdack D004 (US); Mallotus philippensis (Lam.) Müll. Arg., Wurdack D822 (US); Manniophyton africanum Müll. Arg., White 3366 (MO); Maprounea guianensis Aubl., Wurdack D332 (US); Melanolepis multiglandulosa Reichb. & Zoll., Motley 2493 (NY); Micrococca capensis (Baill.) Prain, Kurzweil 463/89 (K). Monadenium guentheri Pax, Chase 1007 (K); Monotaxis grandiflora Endl., Horn 2386 (DUKE); Moultonianthus leembruggianus (Boerl. & Koord.) Steenis, Challen et al. 3 (K); Nealchornea yapurensis Huber, Fine s.n. (US); Neoboutonia mannii Benth. & Hook. f., Fay 6701 (MO); Neoscortechinia kingii (Hook. f.) Pax & K. Hoffm., Chase 1265 (K) GenBank EU293936; Neoshirakia japonica (Siebold & Zucc.) Esser, Wurdack D005 (US); Omphalea diandra L., Chase 570 (K); Ostodes paniculata Blume, Chase 1267 (K); Pachystroma longifolium (Nees) I. M. Johnst., Prince s.n. (US); Pausandra martinii Baill., Berry 7466 (MO); Pedilanthus tithymaloides (L.) Poit., Wurdack D034 (US); Pera bicolor (Klotzsch) Müll. Arg., Gillespie 4300 (US), GenBank EU293937 Pimelodendron zoanthogyne J.J. Sm., Chase 1268 (K); Plukenetia volubilis L., Armbruster 38 (?); Pogonophora schomburgkiana Miers ex Benth., Larpin 1022 (US); Pseudosenefeldera inclinata (Müll. Arg.) Esser, Wurdack D385 (US); Ricinocarpos tuberculatus Müll. Arg., Chase 2164 (K); Ricinodendron heudelotii (Baill.) Heckel, Chase 1269 (K); Ricinus communis L., Wurdack D009 (US); Seidelia triandra (E. Mey.) Pax, Giess 13381 (MO); Senefelderopsis croizatii Steyerm., Berry s.n. (MO); Spathiostemon javensis Blume, Chase 1261 (K); Stillingia sylvatica L. subsp. tenuis (Small) D. J. Rogers, Wurdack D117 (US); Strophioblachia fimbricalyx Boerl., Chase 1270 (K); Sumbaviopsis albicans (Blume) J.J. Sm., Chase 1271 (K); Suregada glomerulata (Blume) Baill., Chase 1272 (K); Synadenium grantii Hook. f., Wurdack D259 (US); Syndyophyllum occidentale (Airy Shaw) Welzen, Aik et al. SAN-111913 (L); Tannodia cordifolia (Baill.) Baill., Ralimanana 293 (K); Tetrorchidium cf. macrophyllum Müll. Arg., Bell et al. 93-204 (US), GenBank EU293938; Tragia fallax Müll. Arg., Bell et al. 94-378 (US); Tragia urticifolia Michx., Wurdack D074 (US); Tragiella anomala (Prain) Pax & K. Hoffm., Mwasumbi et al. 16202 (MO); Trewia nudiflora L., Chase 1273 (K); Triadica sebifera (L.) Small, Wurdack D059 (US); Trigonostemon verrucosus J. J. Sm., Chase 1274 (K); Vernicia montana Lour., Chase 2105 (K). Euphroniaceae: Euphronia guianensis (R. H. Schomb.) H. Hallier, Mori 23699 (NY). Goupiaceae: Goupia glabra Aubl., Prevost 3031 (CAY). Humiriaceae: Humiria wurdackii Cuatrec., Wurdack s.n. (US); Sacoglottis gabonensis Urb., Stone 3283 (MO); Vantanea guianensis Aubl., Pennington 13855 (K). Hypericaceae: Cratoxylum formosum (Jack) Benth & Hook. f. ex Dyer, Chase 1218 (K). Irvingiaceae: Irvingia malayana Oliv., Simpson 2638 (K?); Klainedoxa gabonensis Pierre, Bradley et al. 1092 (MO). Ixonanthaceae: Cyrillopsis paraensis Kuhlm., Hentrich 68 (NY); Ochthocosmus longipedicellatus Steyerm. & Luteyn, Berry 6561 (MO). Lacistemataceae: Lacistema aggregatum Rusby, Pennington et al. 583 (K); Lozania pittieri (Blake) L. B. Sm., Pennington et al. 584 (K). Linaceae: Durandea pentagyna K. Schum., Takeuchi 7103 (MO); Linum perenne L., Chase 111 (NCU); Reinwardtia indica Dumort., Chase 230 (NCU). Malpighiaceae: Dicella nucifera Chodat, Anderson 13607 (MICH); Galphimia gracilis Bartl., Adelson s.n. (MICH), GenBank EU293939. Medusagynaceae: Medusagyne oppositifolia Baker, Fay s.n. (K) [Kew 1981-2059]. Ochnaceae s.s.: Elvasia calophyllea DC., Amaral s.n. (K?); Lophira lanceolata Tiegh., Schmidt 1902 (MO); Ochna multiflora DC., Chase 229 (NCU). Pandaceae: Galearia filiformis (Blume) Boerl., Chase 1334 (K); Microdesmis pierlotiana J. Léonard, Gereau et al. 5654 (MO); Panda oleosa Pierre., Schmidt et al. 2048 (MO). Phyllanthaceae: Amanoa strobilacea Müll. Arg., McPherson 16826 (MO); Apodiscus chevalieri Hutch., Schmidt et al. 2094 (MO); Aporusa frutescens Blume, Chase 1251 (K); Astrocasia neurocarpa (Müll. Arg.) I. M. Johnst. ex Standl., Wurdack D743 (US); Bischofia javanica Blume, Levin 2200 (SD), GenBank EU293940; Cleistanthus oblongifolius (Roxb.) Müll. Arg., Chase 1257 (K); Croizatia brevipetiolata (Secco) Dorr, Dorr et al. 8555 (US), GenBank EU293941; Didymocistus chrysadenius Kuhlm., Gillespie et al. 4805 (US); Discocarpus essequeboensis Klotzsch, Hoffman 996 (US); Gonatogyne brasiliensis (Baill.) Müll. Arg., Cordeiro & Esteves 1384 (K); Heywoodia lucens Sim, Saufferer & Muchai SS-1544 (US); Hieronyma oblonga (Tul.) Müll. Arg., Bell 94-252 (US); Hymenocardia acida Tul., Walters et al. 897 (MO); Lachnostylis bilocularis R. A. Dyer, Kurzweil 83/88 (K); Leptonema glabrum (Leandri) Leandri, McPherson & Rabenantoandro 18389 (MO); Maesobotrya vermeulenii (de Wild.) J. Léonard, Bradley et al. 1032 (MO); Poranthera huegelii Klotzsch, Spjut 7369 (US); Richeria grandis Vahl, Merello et al. 1714 (MO); Sauropus racemosus Beille, Soejarto et al. 10648 (NY); Spondianthus preussii Engl., Merello et al. 1661 (MO); Zimmermania ovata E.A. Bruce, Faden s.n. (US). Picrodendraceae: Androstachys johnsonii Prain, Chase 1904 (K); Hyaenanche globosa (Gaertn.) Lamb. & Vahl, Chase 1445 (K); Picrodendron baccatum Krug & Urb. ex Urban, Wurdack D050; Podocalyx loranthoides Klotzsch, Berry & Aymard 7226 (MO), GenBank EU293955 (partial sequence not used in phylogenetic analyses); Tetracoccus dioicus Parry, Levin 2202 (DUKE), GenBank EU293942. Podostemaceae: Marathrum c.f. oxycarpum Tul., Gabriel da Cachoeirc 9/1996 (AM); Podostemum ceratophyllum Michx., Horn & Wurdack s.n. (DUKE). Putranjivaceae: Drypetes capillipes Pax & K. Hoffm., Harris 4884 (K); Drypetes fallax Pax & K. Hoffm., Harris 4892 (K); Drypetes macrostigma J.J. Sm., Chase 1259 (K); Putranjiva roxburghii Wall., Wurdack D057 (US), GenBank EU293956 (partial sequence not used in phylogenetic analyses). Quiinaceae: Quiina pteridophylla (Radlk.) Pires, Pires s.n. (CPATU) Touroulia guianensis Aubl., Pires (CPATU). Rhizophoraceae s.s.: Bruguiera gymnorhiza Lam., Chase 12838 (K); Carallia brachiata (Lour.) Merr., Chase 2151 (K); Crossostylis multiflora Brongn. & Gris ex Pancher & Sebert, Lowry 5686 (MO); Paradrypetes subintegrifolia G. A. Levin, Acevedo-Rdgz. & Cedeño 7560 (US); Cassipourea lanceolata Tul., Schatz 3689 (MO). Salicaceae s.l.: Abatia parviflora Ruiz & Pav., Pennington 676 (K); Casearia nitida Jacq., FTG 72496; Flacourtia jangomas Steud., Chase 2150 (K); Idesia polycarpa Maxim., Wurdack D22 (US); Poliothyrsis sinensis Oliver, Wurdack D029 (US); Scyphostegia borneensis Stapf, Beaman 911 (BH). Trigoniaceae: Trigoniastrum hypoleucum Miq., Og B128 (L). Violaceae: Hybanthus concolor Spreng., Wurdack D148 (US); Hymenanthera alpina Oliv., Chase 501 (K); Rinorea bengalensis Kuntze, Chase 2148 (K).

(ii) Other related rosids (Celastrales, Oxalidales + Huaceae)

Brunelliaceae: Brunellia acutangula Humb. & Bonpl., Stergios 20646 (US), GenBank EU293943. Celastraceae: Brexia madagascariensis Thouars, Wurdack D764 (US); Maytenus senegalensis (Lam.) Exell, Collenette 4/93 (K); Plagiopteron suaveolens Griff., Chase 1335 (K); Siphonodon celastrineus Griff., Chase 2097 (K); Stackhousia minima Hook. f., Molloy s.n. (CHR); Tripterygium regelii Sprague & Takeda, Chase 1003 (K). Cephalotaceae: Cephalotus folicularis Labill., Chase 147 (NCU). Connaraceae: Rourea minor Leenh., Chase 1221 (K). Cunoniaceae: Eucryphia milliganii Hook. f., Chase 2528 (K). Elaeocarpaceae: Crinodendron hookerianum Gay, Chase 909 (K); Sloanea sp., Chase 343 (NCU). Huaceae: Afrostyrax sp., Cheek 5007 (K). Lepidobotryaceae: Ruptiliocarpon caracolito Hammel & Zamora, Hammel 19102 (MO). Oxalidaceae: Averrhoa carambola L., Chase 214 (NCU). Parnassiaceae: Parnassia grandifolia DC., Wurdack D795 (US), GenBank EU293944.

Intron absent

(i) Malpighiales

Elatinaceae: Elatine hexandra DC., Chase 2978 (K), GenBank EU293945. Euphorbiaceae s.s.: Cnidoscolus urens (L.) Arthur var. stimulosus (Michx.) Govaerts, Wurdack D002 (US); Elateriospermum tapos Blume, Soepadmo & Suhaimi s193 (NY), GenBank EU293946; Glycydendron amazonicum Ducke, Gillespie et al. 4546 (US); Glycydendron cf. amazonicum Ducke, Mori et al. 23265 (US); Hevea sp. [cf. pauciflora (Spruce ex Benth.) Müll. Arg.], Gillespie 4272 (US), GenBankEU293947; Manihot esculenta subsp. esculenta Crantz, EU117376; Manihot foetida Pohl, Olsen s.n.; Manihot grahamii Hook., Wurdack s.n. (US); Manihot pauciflora Brandegee, Villasenor 1248 (NY); Manihot walkerae Croizat, Olsen s.n.; Micrandra inundata P. E. Berry & A. Wiedenhoeft, Berry 6350 (MO). Lophopyxidaceae: Lophopyxis maingayi Hook. f., Adelbai P-10203 (US), GenBank EU293948. Malesherbiaceae: Malesherbia weberbaueri Gilg, Weigend 2000/365 (NY), GenBank EU293949. Passifloraceae s.s.: Paropsia madagascariensis (Baill.) H. Perrier, Zyhra 949 (WIS); Passiflora coccinea Aubl., Chase 2475 (K), GenBank EU293950. Phyllanthaceae: Breynia disticha J. R. Forst. & G. Forst. cv. ‘Rosea Picta’, Wurdack D012 (US); Flueggea virosa (Roxb. ex. Willd.) Voigt subsp. virosa, Wurdack D101 (US); Glochidion puberum (L.) Hutch., Wurdack D003 (US); Leptopus colchicus (Fisch. & C. A. Mey. ex Boiss.) Pojark., Wurdack D778 (US), GenBank EU293951; Leptopus esquirolii (H. Lév.) P. T. Li, 1980 Sino-American Bot. Exped. 1678 (US); Margaritaria tetracocca (Baill.) G. L. Webster, Wurdack D044 (US); Phyllanthus epiphyllanthus L., Wurdack D056 (US), GenBank EU293952; Phyllanthus fluitans Benth. ex Müll. Arg., Wurdack D761 (US); Phyllanthus juglandifolius Willd., Wurdack D759 (US); Phyllanthus nutans Sw., Wurdack D762 (US); Reverchonia arenaria A. Gray, Atwood 17245 (NY); Savia bahamensis Britton, Wurdack D048 (US). Picrodendraceae: Austrobuxus megacarpus P. I. Forster, Forster 21239 (BRI), GenBank EU293953; Choriceras majus Airy Shaw, Forster 21230 (BRI); Dissiliaria muelleri Baill., Forster 14629 (BRI); Whyanbeelia terrae-reginae Airy Shaw & B. Hyland, Forster 21231 (BRI). Turneraceae: Tricliceras longipedunculatum (Mast.) R. Fern., Kanji et al. 304 (NY); Turnera ulmifolia L., Wurdack s.n. (US), GenBank EU293954.

(ii) Other related rosids (Celastrales, Oxalidales + Huaceae): none noted.

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Daniell, H., Wurdack, K.J., Kanagaraj, A. et al. The complete nucleotide sequence of the cassava (Manihot esculenta) chloroplast genome and the evolution of atpF in Malpighiales: RNA editing and multiple losses of a group II intron. Theor Appl Genet 116, 723–737 (2008). https://doi.org/10.1007/s00122-007-0706-y

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