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Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny

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Abstract

The exact phylogenetic position of Gnetales, a small, highly modified group of gymnosperms with an accelerated rate of molecular evolution, is one of the most challenging issues for seed plant systematics. Recent results from entire plastid genome (ptDNA) sequencing revealed the absence of the entire suite of plastid ndh genes in several species of Gnetales and the pine family (Pinaceae) potentially highlighting a major structural feature linking these two groups—concerted loss of all plastid genes for the NADH dehydrogenase complex. However, the precise extent of ndh gene loss in gymnosperms has not been surveyed. Using a slot-blot hybridization method, we probed all 11 ndh genes in 162 species from 70 of 85 gymnosperm genera. We find that all ndh genes are absent across Gnetales and Pinaceae, but not in any other group of gymnosperms. This feature represents either a major synapomorphy for a clade consisting of these two lineages or, less likely, a convergent loss. Our survey substantially extends previous inferences based on more limited sampling and, if the former evolutionary interpretation is correct, it provides additional support for the contentious “gnepine” hypothesis, which places Gnetales as sister to Pinaceae.

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References

  • Adams KL, Qiu YL, Stoutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci 99:9905–9912

    Article  PubMed  CAS  Google Scholar 

  • Albert VA, Backlund A, Bremer K, Chase MW, Manhardt JR, Mishler BD, Nixon KC (1994) Functional constraints and rbcL evidence for land plant phylogeny. Ann Mo Bot Gard 81:534–567

    Article  Google Scholar 

  • Bailey CD, Doyle JJ, Kajita T, Nemoto T, Ohashi H (1997) The chloroplast rpl2 intron and ORF184 as phylogenetic markers in the legume tribe Desmodieae. Syst Bot 22:133–138

    Article  Google Scholar 

  • Bennoun P (2002) The present model for cholororespiration. Photosynthesis Res 73:273–277

    Article  CAS  Google Scholar 

  • Bowe LM, Coat G, dePamphilis CW (2000) Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci 97:4092–4097

    Article  PubMed  CAS  Google Scholar 

  • Bukhov N, Carpentier R (2004) Alternative photosystem I-driver electron transport routes: mechanisms and functions. Photosynthesis Res 82:17–33

    Article  CAS  Google Scholar 

  • Bungard RA (2004) Photosynthetic evolution in parasitic plants: insight from the cholorplast genome. Bioassays 26:235–247

    Article  CAS  Google Scholar 

  • Burleigh JG, Mathews S (2004) Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. Am J Bot 91:235–237

    Article  Google Scholar 

  • Burleigh JG, Mathews S (2007a) Assessing among-locus variation in the inference of seed plant phylogeny. Int J Plant Sci 168(2):111–124

    Article  CAS  Google Scholar 

  • Burleigh JG, Mathews S (2007b) Assessing systematic error in the inference of seed plant phylogeny. Int J Plant Sci 168(2):125–135

    Article  CAS  Google Scholar 

  • Casano LM, Martín M, Sabater B (2001) Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley. Plant Physiol 125:1450–1458

    Article  PubMed  CAS  Google Scholar 

  • Chang C-C, Lin H-C, Lin I-P, T-Y Chow, Chen H-H, Chen W-H, Cheng C-H, Lin C-Y, Liu S-M, Chang C-C, Chaw S-M (2006) The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol 23:279–291

    Article  PubMed  CAS  Google Scholar 

  • Chaw S-M, Aharkikh A, Sung H-M, Lau T-C, Li W-H (1997) Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA squences. Mol Biol Evol 14:56–68

    PubMed  CAS  Google Scholar 

  • Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer JD (2000) Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc Natl Acad Sci 97:4086–4091

    Article  PubMed  CAS  Google Scholar 

  • Chumley TW, McCoy SKR, Raubeson LA (2008) Gne-deep: exploring Gnetalean affinities in seed plant phylogeny with 83 plastid genes. Botany 2008: Joint Annual Meeting of Canadian Botanical Association, American Fern Society, American Society of Plant Taxonomists, and the Botanical Society of America, Vancouver, BC, Canada [http://2008.botanyconference.org/engine/search/index.php?func=detail&aid=770]

  • Clegg MT, Gaut BS, Learn GH, Morton BR (1994) Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci 91:6795–6801

    Article  PubMed  CAS  Google Scholar 

  • Crane PR (1985) Phylogenetic analysis of seed plants and the origin of angiosperms. Ann Mo Bot Gard 72:716–793

    Article  Google Scholar 

  • Cronn R, Liston A, Parks M, Gernandt DS, Shen R, Mockler T (2008) Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Res 36(19):e122

    Article  PubMed  Google Scholar 

  • dePamphilis CW, Palmer JD (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348 (22):337–339

    Google Scholar 

  • Diaz M, de Haro V, Munoz R, Quiles MJ (2007) Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant Cell Environ 30:1578–1585

    Article  PubMed  CAS  Google Scholar 

  • Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JA (eds) Molecular systematics of plants. Chapman & Hall, New York, pp 14–35

    Google Scholar 

  • Downie SR, Olmstead RG, Zurawski G, Soltis DE, Soltis PS, Watson JC, Palmer JD (1991) Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications. Evolution 45:1245–1259

    Article  CAS  Google Scholar 

  • Doyle JA (2006) Seed ferns and the origin of angiosperms. J Torrey Bot Soc 133:169–209

    Article  Google Scholar 

  • Doyle JA, Donoghue MJ (1986) Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot Rev 52:321–431

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Doyle JJ, Doyle JL, Palmer JD (1995) Multiple independent losses of two genes and one intron from legume chloroplast genomes. Mol Phylogenet Evol 5:429–438

    Article  Google Scholar 

  • Doyle JJ, Doyle JL, Ballenger JA, Palmer JD (1996) The distribution and phylogenetic significance of a 50-kb chloroplast DNA inversion in the flowering plant family Leguminosae. Syst Bot 20:272–294

    Article  Google Scholar 

  • Endo T, Ishida S, Ishikawa N, Sato F (2008) Chloroplastic NAD(P)H dehydrogenase complex and cyclic electron transport around photosystem I. Mol Cells 25:158–162

    PubMed  CAS  Google Scholar 

  • Feild TS, Brodribb TJ (2005) A unique mode of parasitism in the conifer coral tree Parasitaxus ustus (Podocarpaceae). Plant Cell Environ 28:1316–1325

    Article  CAS  Google Scholar 

  • Felsenstein J (1983) Parsimony in systematics: biological and statistical issues. Annu Rev Ecol Syst 14:313–333

    Article  Google Scholar 

  • Frolich MW, Parker DS (2000) The mostly male theory of flower evolutionary origins: from genes to fossils. Syst Bot 25(2):155–170

    Article  Google Scholar 

  • Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:45

    Article  PubMed  Google Scholar 

  • Goremykin V, Bobrova V, Pahnke J, Troitsky A, Antonov A, Martin W (1996) Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. Mol Biol Evol 13:383–396

    PubMed  CAS  Google Scholar 

  • Graham SW, Iles WJD (2009) Different gymnosperm outgroups have (mostly) congruent signal regarding the root of flowering plant phylogeny. Am J Bot 96:216–227

    Article  Google Scholar 

  • Graham SW, Olmstead RG (2000a) Evolutionary significance of an unusual chloroplast DNA inversion found in two basal angiosperm lineages. Curr Genet 37:183–188

    Article  PubMed  CAS  Google Scholar 

  • Graham SW, Olmstead RG (2000b) Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am J Bot 87:1712–1730

    Article  PubMed  CAS  Google Scholar 

  • Gugerli F, Sperisen C, Buchler U, Brunner L, Brodbeck S, Palmer JD, Qiu YL (2001) The evolutionary split of Pinaceae from other conifers: evidence from an intron loss and a multigene phylogeny. Mol Phylogen Evol 21:167–175

    Article  CAS  Google Scholar 

  • Hamby RK, Zimmer EA (1992) Ribosomal RNA as a phylogenetic tool. In: Soltis PE, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman & Hall, London, pp 50–91

    Google Scholar 

  • Hasebe M, Kofugi R, Ito M, Kato M, Iwatsuki K, Ueda K (1992) Phylogeny of gymnosperms inferred from rbcL gene sequence. J Plant Res 105:673–679

    CAS  Google Scholar 

  • Hendy MD, Penny D (1989) A framework for the quantitative study of evolutionary trees. Syst Zool 38:296–309

    Google Scholar 

  • Hirao T, Watanabe A, Kurita M, Kondo T (2008) Complete nucleotide sequence of the Cryptomeria japonica D. Don. chloroplast genome and comparative chloroplast genomics: diversified genomic structure of coniferous species. BMC Plant Biol 8:70

    Article  PubMed  Google Scholar 

  • Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci 104:19369–19374

    Article  PubMed  CAS  Google Scholar 

  • Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2002) Plant systematics: a phylogenetic approach, 2nd edn. Sinauer Associates, Sunderland, p 576

    Google Scholar 

  • Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121

    Article  PubMed  CAS  Google Scholar 

  • Leebens-Mack J, Raubeson LA, Cui LY, Kuehl JV, Fourcade MH, Chumley TW, Boore JL, Jansen RK, dePamphilis CW (2005) Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one’s way out of the Felsenstein zone. Mol Biol Evol 22:1948–1963

    Article  PubMed  CAS  Google Scholar 

  • Loconte H, Stevenson DW (1990) Cladistics of the Spermatophyta. Brittonia 42:197–211

    Article  Google Scholar 

  • Magallón S, Sanderson MJ (2002) Relationships among seed plants inferred from highly conserved genes: sorting conflicting phylogenetic signals among ancient lineages. Am J Bot 89:1991–2006

    Article  Google Scholar 

  • Mathews S (2009) Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. Am J Bot 96(1):228–236

    Article  Google Scholar 

  • Mathews S, Donoghue MJ (2000) Basal angiosperm phylogeny inferred from duplicate phytochromes A and C. Int J Plant Sci 161:S41–S55

    Article  Google Scholar 

  • McCoy SR, Kuehl JV, Boore JL, Raubeson LA (2008) The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol 8:130

    Article  PubMed  Google Scholar 

  • McNeal JR, Kuehl JV, Boore JL, dePamphilis CW (2007) Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biol 7:57

    Article  PubMed  Google Scholar 

  • McPherson MA, Fay ME, Chase MW, Graham SW (2004) Parallel loss of a slowly evolving intron from two closely related families in asparagales. Syst Bot 29:296–307

    Article  Google Scholar 

  • Moreira D, Philippe H (2000) Molecular phylogeny: pitfalls and progress. Int Microbiol 3:9–16

    PubMed  CAS  Google Scholar 

  • Nickrent DL, Parkinson CL, Palmer JD, Duff RJ (2000) Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol Biol Evol 17:1885–1895

    PubMed  CAS  Google Scholar 

  • Nixon KC, Crepet WL, Stevenson D, Friis EM (1994) A reevaluation of seed plant phylogeny. Ann Mo Bot Gard 81:484–533

    Article  Google Scholar 

  • Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481

    Article  Google Scholar 

  • Olmstead RG, dePamphilis CW, Wolfe AD, Young ND, Elisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348–361

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Bogarad L, Vasil IK (eds) Cell culture and somatic cell genetics of plants 7A. Academic, San Diego, pp 6–53

    Google Scholar 

  • Palmer JD, Soltis DE, Chase MW (2004) The plant tree of life: an overview and some points of view. Am J Bot 91:1437–1445

    Article  Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550

    Article  PubMed  CAS  Google Scholar 

  • Plunkett GM, Downie SR (2000) Expansion and contraction of the chloroplast inverted repeat in Apiaceae subfamily Apioideae. Syst Bot 25:648–667

    Article  Google Scholar 

  • Qiu Y-L, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson RW, Hendry TA, Taylor DW, Testa CM, Ambros M (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708

    Article  CAS  Google Scholar 

  • Rai HS, O‘Brien HE, Reeves PA, Olmstead RG, Graham SW (2003) Inference of higher-order relationships in the cycads from a large chloroplast data set. Mol Phylogen Evol 29:350–359

    Article  CAS  Google Scholar 

  • Rai HS, Reeves PA, Peakall R, Olmstead RG, Graham SW (2008) Inference of higher-order conifer relationships from a multi-locus plastid data set. Botany 86:658–669

    Article  CAS  Google Scholar 

  • Raubeson LA, Jansen RK (1992) A rare chloroplast DNA structural mutation is shared by all conifers. Biochem Syst Ecol 20:17–24

    Article  CAS  Google Scholar 

  • Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459

    Article  PubMed  Google Scholar 

  • Romeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PS I during photosynthesis and plant stress response. Plant Cell Environ 104:1–1051

    Google Scholar 

  • Rydin C, Källersjö M (2002) Taxon sampling and seed plant phylogeny. Cladistics 18:485–513

    Google Scholar 

  • Rydin C, Källersjö M, Friis EM (2002) Seed plant relationships and the systematic position of Gnetales based on nuclear and chloroplast DNA: conflicting data, rooting problems, and the monophyly of conifers. Int J Plant Sci 163:197–214

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Samigullin TK, Martin WF, Troitsky AV, Antonov AS (1999) Molecular data from the chlorplast rpoC1 gene suggest a deep and distinct dichotomy of contemporary spermatophytes into two monophyla: gymnosperms (including Gnetalaes) and angiosperms. J Mol Evol 49:310–315

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchishinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    PubMed  CAS  Google Scholar 

  • Sinclair WT, Mill RR, Gardner MF, Woltz P, Jaffré T, Preston J, Hollingsworth ML, Ponge A, Möller M (2002) Evolutionary relationships of the New Caledonian heterotrophic conifer, Parasitaxus usta (Podocarpaceae), inferred from chloroplast trnL-F intron/spacer and nuclear rDNA ITS2 sequences. Plant Syst Evol 233:79–104

    Article  CAS  Google Scholar 

  • Soltis PS, Soltis DE, Savolainen V, Crane PR, Barraclough TG (2002) Rate heterogeneity among lineages of tracheophytes: integration of molecular and fossil data and evidence for molecular living fossils. Proc Natl Acad Sci 99:4430–4435

    Article  PubMed  CAS  Google Scholar 

  • Stefanović S, Olmstead RG (2005) Down the slippery slope: plastid genome evolution in Convolvulaceae. J Mol Evol 61:292–305

    Article  PubMed  Google Scholar 

  • Stefanović S, Jager M, Deutsch J, Broutin J, Masselot M (1998) Phylogenetic relationships of conifers inferred from partial 28S rRNA gene sequences. Am J Bot 85:688–697

    Article  Google Scholar 

  • Tallon C, Quiles MJ (2007) Acclimation to heat and high light intensity during the development of oat leaves increases the NADH DH complex and PTOX levels in chloroplasts. Plant Sci 173:438–445

    Article  CAS  Google Scholar 

  • Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci 91:9794–9798

    Article  PubMed  CAS  Google Scholar 

  • Wettstein RR (1907) Handbuch der Systematischen Botanik. Franz Deuticke, Leipzig

    Google Scholar 

  • Wickett NJZY, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, dePamphilis CW, Boore JL, Goffinet B (2008) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25(2):393–411

    Article  PubMed  CAS  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058

    Article  PubMed  CAS  Google Scholar 

  • Wu C-S, Wang Y-N, Liu S-M, Chaw S-M (2007) Chloroplast genome (cpDNA) of Cycas taitungensis and 56 cp protein-coding genes of Gnetum parvifolium: insights into cpDNA evolution and phylogeny of extant seed plants. Mol Biol Evol 24:1366–1379

    Article  PubMed  CAS  Google Scholar 

  • Wu C-S, Lai Y-T, Lin C-P, Wang Y-N, Chaw S-M (2009) Evolution of reduced and compact chloroplast genomes (cpDNAs) in gnetophytes: selection towards a lower cost strategy. Mol Phylogen Evol (in press)

  • Zapata JM, Guéra A, Esteban-Carrasco A, Martín M, Sabater JM (2005) Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ 12:1277–1284

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

For providing generous access to their live plant collections, the authors are grateful to directors/managers of the following institutions: Humboldt State University (Acrata, CA) greenhouse, Indiana University (Bloomington, IN) greenhouse, University of Alberta (Edmonton, AB) greenhouse, University of Toronto (Toronto, ON) greenhouse, University of Washington (Seattle, WA) greenhouse and Arboretum, University of Guelph Arboretum (Guelph, ON), Devonian Botanic Garden (Devon, AB), Jardin botanique de Montréal (Montréal, QC), University of Belgrade Arboretum (Belgrade, Serbia), Vienna Botanical Garden (Vienna, Austria), and Carleton University (Ottawa, ON) greenhouse. We also thank curators/directors of ALTA, IND, and TRT for supplying plant material. Special thanks are due to Sean Graham and two anonymous reviewers for their valuable suggestions that improved the earlier versions of the manuscript. Financial support from the Natural Sciences and Engineering Research Council of Canada, Canada Foundation for Innovation and Ontario Research Funds to S. Stefanović is gratefully acknowledged.

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Braukmann, T.W.A., Kuzmina, M. & Stefanović, S. Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet 55, 323–337 (2009). https://doi.org/10.1007/s00294-009-0249-7

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