Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat.

UNLABELLED • PREMISE OF THE STUDY Land-plant plastid genomes have only rarely undergone significant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes.• METHODS Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR).• KEY RESULTS The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (∼113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact.• CONCLUSIONS The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) complex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.

[1]  S. Magallón,et al.  A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. , 2015, The New phytologist.

[2]  Tae-Jin Yang,et al.  Comprehensive Survey of Genetic Diversity in Chloroplast Genomes and 45S nrDNAs within Panax ginseng Species , 2015, PloS one.

[3]  Jeremy J. W. Chen,et al.  NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss , 2015, BMC Plant Biology.

[4]  Yinlong Xie,et al.  Dissecting Molecular Evolution in the Highly Diverse Plant Clade Caryophyllales Using Transcriptome Sequencing , 2015, Molecular biology and evolution.

[5]  C. Osborne,et al.  Genetic enablers underlying the clustered evolutionary origins of C4 photosynthesis in angiosperms. , 2015, Molecular biology and evolution.

[6]  G. Wong,et al.  The location and translocation of ndh genes of chloroplast origin in the Orchidaceae family , 2015, Scientific Reports.

[7]  M. Logacheva,et al.  Exploring the Limits for Reduction of Plastid Genomes: A Case Study of the Mycoheterotrophic Orchids Epipogium aphyllum and Epipogium roseum , 2015, Genome biology and evolution.

[8]  Tracey A Ruhlman,et al.  Evolutionary and biotechnology implications of plastid genome variation in the inverted-repeat-lacking clade of legumes. , 2014, Plant biotechnology journal.

[9]  Jin-Hua Ran,et al.  Evolution and biogeography of gymnosperms. , 2014, Molecular phylogenetics and evolution.

[10]  L. Eguiarte,et al.  Beyond aridification: multiple explanations for the elevated diversification of cacti in the New World Succulent Biome. , 2014, The New phytologist.

[11]  Xiaolong Wu,et al.  BLESS: Bloom filter-based error correction solution for high-throughput sequencing reads , 2014, Bioinform..

[12]  T. Drezner The keystone saguaro (Carnegiea gigantea, Cactaceae): a review of its ecology, associations, reproduction, limits, and demographics , 2014, Plant Ecology.

[13]  T. Shikanai,et al.  Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. , 2014, Current opinion in biotechnology.

[14]  R. Jansen,et al.  Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. , 2014, Molecular biology and evolution.

[15]  S. Salzberg,et al.  Sequencing and Assembly of the 22-Gb Loblolly Pine Genome , 2014, Genetics.

[16]  Daniel B. Sloan,et al.  A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). , 2014, Molecular phylogenetics and evolution.

[17]  C. dePamphilis,et al.  Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. , 2014, Molecular biology and evolution.

[18]  Yan Zhang,et al.  Mechanisms of Functional and Physical Genome Reduction in Photosynthetic and Nonphotosynthetic Parasitic Plants of the Broomrape Family[W][OPEN] , 2013, Plant Cell.

[19]  D. Les,et al.  The Plastid Genome of Najas flexilis: Adaptation to Submersed Environments Is Accompanied by the Complete Loss of the NDH Complex in an Aquatic Angiosperm , 2013, PloS one.

[20]  D. Leister,et al.  Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants , 2013, Front. Plant Sci..

[21]  Marc Lohse,et al.  OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets , 2013, Nucleic Acids Res..

[22]  Paul D. Shaw,et al.  Using Tablet for visual exploration of second-generation sequencing data , 2013, Briefings Bioinform..

[23]  D. Leister,et al.  PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. , 2013, Molecular cell.

[24]  Masato Nakai,et al.  Uncovering the Protein Translocon at the Chloroplast Inner Envelope Membrane , 2013, Science.

[25]  S. Stefanović,et al.  Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss , 2013, Journal of experimental botany.

[26]  E. Kejnovský,et al.  Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization , 2013, Heredity.

[27]  T. Kohchi,et al.  Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. , 2012, The Plant journal : for cell and molecular biology.

[28]  B. Faircloth,et al.  Primer3—new capabilities and interfaces , 2012, Nucleic acids research.

[29]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[30]  S. Stefanović,et al.  Plastid genome evolution in mycoheterotrophic Ericaceae , 2012, Plant Molecular Biology.

[31]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[32]  Ching-Ping Lin,et al.  Loss of Different Inverted Repeat Copies from the Chloroplast Genomes of Pinaceae and Cupressophytes and Influence of Heterotachy on the Evaluation of Gymnosperm Phylogeny , 2011, Genome biology and evolution.

[33]  T. Shikanai,et al.  Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. , 2011, Plant & cell physiology.

[34]  T. Shikanai,et al.  Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. , 2011, Biochimica et biophysica acta.

[35]  J. Timmis,et al.  The origin and characterization of new nuclear genes originating from a cytoplasmic organellar genome. , 2011, Molecular biology and evolution.

[36]  T. Markow,et al.  Phylogeography of the Cactophilic Drosophila and Other Arthropods Associated with Cactus Necroses in the Sonoran Desert , 2011, Insects.

[37]  U. Eggli,et al.  Contemporaneous and recent radiations of the world's major succulent plant lineages , 2011, Proceedings of the National Academy of Sciences.

[38]  T. Shikanai,et al.  An Src Homology 3 Domain-Like Fold Protein Forms a Ferredoxin Binding Site for the Chloroplast NADH Dehydrogenase-Like Complex in Arabidopsis[W] , 2011, Plant Cell.

[39]  Kai F. Müller,et al.  The evolution of the plastid chromosome in land plants: gene content, gene order, gene function , 2011, Plant Molecular Biology.

[40]  R. Jansen,et al.  Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae) , 2011, Plant Molecular Biology.

[41]  J. Palmer,et al.  Localized hypermutation and associated gene losses in legume chloroplast genomes. , 2010, Genome research.

[42]  A. Búrquez,et al.  Geographic variation in reproductive success of Stenocereus thurberi (Cactaceae): Effects of pollination timing and pollinator guild. , 2010, American journal of botany.

[43]  W. M. Whitten,et al.  Evolution along the crassulacean acid metabolism continuum , 2010 .

[44]  Bartolomé Sabater,et al.  Plastid ndh genes in plant evolution. , 2010, Plant physiology and biochemistry : PPB.

[45]  J. G. Burleigh,et al.  Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots , 2010, Proceedings of the National Academy of Sciences.

[46]  U. Eggli,et al.  Disintegrating Portulacaceae: a new familial classification of the suborder Portulacineae (Caryophyllales) based on molecular and morphological data , 2010 .

[47]  Ching-Ping Lin,et al.  Evolution of reduced and compact chloroplast genomes (cpDNAs) in gnetophytes: selection toward a lower-cost strategy. , 2009, Molecular phylogenetics and evolution.

[48]  Saša Stefanović,et al.  Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny , 2009, Current Genetics.

[49]  R. Jansen,et al.  Extensive Reorganization of the Plastid Genome of Trifolium subterraneum (Fabaceae) Is Associated with Numerous Repeated Sequences and Novel DNA Insertions , 2008, Journal of Molecular Evolution.

[50]  R. Viola,et al.  Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. , 2008, Molecular biology and evolution.

[51]  A. Dhingra,et al.  Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale – A wild ancestor of cultivated buckwheat , 2008, BMC Plant Biology.

[52]  L. Fan,et al.  Chloroplast DNA insertions into the nuclear genome of rice: the genes, sites and ages of insertion involved , 2008, Functional & Integrative Genomics.

[53]  R. Gorelick The Great Cacti: Ethnobotany and Biogeography , 2008 .

[54]  V. Goremykin,et al.  The molecular phylogeny of Rebutia (Cactaceae) and its allies demonstrates the influence of paleogeography on the evolution of South American mountain cacti. , 2007, American journal of botany.

[55]  Chung-Shien Wu,et al.  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. , 2007, Molecular biology and evolution.

[56]  J. Mauseth Structure-function relationships in highly modified shoots of cactaceae. , 2006, Annals of botany.

[57]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[58]  T. Shikanai,et al.  Chloroplastic NAD(P)H Dehydrogenase in Tobacco Leaves Functions in Alleviation of Oxidative Damage Caused by Temperature Stress1[OA] , 2006, Plant Physiology.

[59]  M. Donoghue,et al.  Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. , 2005, American journal of botany.

[60]  W. Martin,et al.  Mutational Decay and Age of Chloroplast and Mitochondrial Genomes Transferred Recently to Angiosperm Nuclear Chromosomes1[w] , 2005, Plant Physiology.

[61]  Junichi Obokata,et al.  The Rice Nuclear Genome Continuously Integrates, Shuffles, and Eliminates the Chloroplast Genome to Cause Chloroplast–Nuclear DNA Fluxw⃞ , 2005, The Plant Cell Online.

[62]  Sergei L. Kosakovsky Pond,et al.  HyPhy: hypothesis testing using phylogenies , 2005, Bioinform..

[63]  M. Sanderson,et al.  A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. , 2004, American journal of botany.

[64]  M. Pagel,et al.  Bayesian estimation of ancestral character states on phylogenies. , 2004, Systematic biology.

[65]  F. Blattner,et al.  Mauve: multiple alignment of conserved genomic sequence with rearrangements. , 2004, Genome research.

[66]  Tsuyoshi Endo,et al.  Cyclic electron flow around photosystem I is essential for photosynthesis , 2004, Nature.

[67]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[68]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[69]  J. Palmer,et al.  Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. , 2003, Molecular phylogenetics and evolution.

[70]  J. N. Holland,et al.  SONORAN DESERT COLUMNAR CACTI AND THE EVOLUTION OF GENERALIZED POLLINATION SYSTEMS , 2001 .

[71]  Lars S. Jermiin,et al.  Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus , 2001, Plant Cell.

[72]  R. Mache,et al.  The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization , 2001, Plant Molecular Biology.

[73]  G. Peltier,et al.  Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. , 2000, Plant physiology.

[74]  Raymond M. Turner,et al.  An 85-year study of saguaro (Carnegiea gigantea) demography , 1998 .

[75]  P. Nixon,et al.  Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes , 1998, The EMBO journal.

[76]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[77]  K. H. Wolfe,et al.  Ebb and flow of the chloroplast inverted repeat , 1996, Molecular and General Genetics MGG.

[78]  S. Muse,et al.  A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. , 1994, Molecular biology and evolution.

[79]  J. Palmer,et al.  A chloroplast DNA phylogeny of the Caryophyllales based on structural and inverted repeat restriction site variation , 1994 .

[80]  M. Pagel Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[81]  P. Nobel,et al.  Effect of Nurse Plants on the Microhabitat and Growth of Cacti , 1989 .

[82]  P. Nobel,et al.  HIGH-TEMPERATURE RESPONSES OF NORTH AMERICAN CACTI' , 1984 .

[83]  R. FitzJohn,et al.  The unsolved challenge to phylogenetic correlation tests for categorical characters. , 2015, Systematic biology.

[84]  J. Betancourt,et al.  Regional demographic trends from long-term studies of saguaro (Carnegiea gigantea) across the northern Sonoran Desert , 2013 .

[85]  L. Eguiarte,et al.  Phylogenetic relationships and evolution of growth form in Cactaceae (Caryophyllales, Eudicotyledoneae). , 2011, American journal of botany.

[86]  R. Nyffeler The closest relatives of cacti: insights from phylogenetic analyses of chloroplast and mitochondrial sequences with special emphasis on relationships in the tribe Anacampseroteae. , 2007, American journal of botany.

[87]  Derrick J. Zwickl Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion , 2006 .

[88]  J. Palmer,et al.  Chloroplast DNA evolution among legumes: Loss of a large inverted repeat occurred prior to other sequence rearrangements , 2004, Current Genetics.

[89]  C. Lottaz,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[90]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .