Abstract
Main conclusion
The leafless and endophytic habitat may significantly relax the selection pressure on photosynthesis, and plastid transcription and translation, causing the loss/pseudogenization of several essential plastid-encoding genes in dwarf mistletoes.
Abstract
Dwarf mistletoes (Arceuthobium spp., Viscaceae) are the most destructive plant parasites to numerous conifer species worldwide. In this study, the plastid genomes (plastomes) of Arceuthobium chinense Lecomte and A. pini Hawksworth and Wiens were sequenced and characterized. Although dwarf mistletoes are hemiparasites capable of photosynthesis, their plastomes were highly degenerated, as indicated by the smallest plastome size, the lowest GC content, and relatively very few intact genes among the Santalales hemiparasites. Unexpectedly, several essential housekeeping genes (rpoA, rpoB, rpoC1, and rpoC2) and some core photosynthetic genes (psbZ and petL), as well as the rpl33 gene, that is indispensable for plants under stress conditions, were deleted or pseudogenized in the Arceuthobium plastomes. Our data suggest that the leafless and endophytic habit, which heavily relies on the coniferous hosts for nutrients and carbon requirement, may largely relax the selection pressure on photosynthesis, as well as plastid transcription and translation, thus resulting in the loss/pseudogenization of such essential plastid-encoding genes in dwarf mistletoes. Therefore, the higher level of plastome degradation in Arceuthobium species than other Santalales hemiparasites is likely correlated with the evolution of leafless and endophytic habit. A higher degree of plastome degradation in Arceuthobium. These findings provide new insights into the plastome degeneration associated with parasitism in Santalales and deepen our understanding of the biology of dwarf mistletoes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The newly sequenced plastomes in this study were deposited in the NCBI GenBank database under the accession number MT635188–MT635189 (Table 1).
References
Ahmed I, Biggs PJ, Matthews PJ, Collins LJ, Hendy MD, Lockhart PJ (2012) Mutational dynamics of aroid chloroplast genomes. Genome Biol Evol 4:1316–1323. https://doi.org/10.1016/bs.abr.2017.11.014
Alkatib S, Scharff LB, Rogalski M, Fleischmann TT, Matthes A, Seeger S, Schötler MA, Ruf S, Bock R (2012) The contributions of wobbling and superwobbling to the reading of the genetic code. PLoS Genet 8:e1003076. https://doi.org/10.1371/journal.pgen.1003076
Alosi MC, Calvin CL (1985) The ultrastructure of dwarf mistletoe (Arceuthobium spp.) sinker cells in the region of the host secondary vasculature. Can J Bot 63:889–898. https://doi.org/10.2307/2996548
Baranyay JA, Hawksworth FG, Smith RB (1971) Glossary of dwarf mistletoe terms. Canadian Forestry Service, Pacific Forest Research Centre, Victoria
Blazier JC, Guisinger-Bellian MM, Jansen RK (2011) Recent loss of plastidencoded ndh genes within Erodium (Geraniaceae). Plant Mol Biol 76:263–272. https://doi.org/10.1007/s11103-011-9753-5
Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH et al (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. https://doi.org/10.1093/molbev/msj029
Chen L, Yu R, Dai J, Liu Y, Zhou R (2020a) The loss of photosynthesis pathway and genomic locations of the lost plastid genes in a holoparasitic plant Aeginetia indica. BMC Plant Biol 20:199. https://doi.org/10.1186/s12870-020-02415-2
Chen XL, Fang DM, Wu CY, Liu B, Liu Y, Sahu SK et al (2020b) Comparative plastome analysis of root-and stem-feeding parasites of Santalales untangle the footprints of feeding mode and lifestyle transitions. Genome Biol Evol 12:3663–3676. https://doi.org/10.1093/gbe/evz271
Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL et al (2006) The complete chloroplast genome sequence of Pelargonium x hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190. https://doi.org/10.1093/molbev/msl089
Coissac E, Hollingsworth PM, Lavergne S, Taberlet P (2016) From barcodes to genomes: extending the concept of DNA barcoding. Mol Ecol 25:1423–1428. https://doi.org/10.1111/mec.13549
Daniel H, Lin CS, Yu M, Chang WJ (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134. https://doi.org/10.1186/s13059-016-1004-2
Der JP, Nickrent DL (2008) A molecular phylogeny of Santalaceae (Santalales). Syst Bot 33:107–116. https://doi.org/10.1600/036364408783887438
Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45:e18. https://doi.org/10.1093/nar/gkw955
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Ehrnthaler M, Scharff LB, Fleischmann TT, Hasse C, Ruf S, Bock R (2014) Synthetic lethality in the tobacco plastid ribosome and its rescue at elevated growth temperatures. Plan Cell 26:765–776. https://doi.org/10.1105/tpc.114.123240
Firetti F, Zuntini AR, Gaiarsa JW, Oliveira RS, Lohmann LG, Van Sluys MA (2017) Complete chloroplast genome sequences contribute to plant species delimitation: a case study of the Anemopaegma species complex. Am J Bot 104:1493–1509
Fleischmann TT, Scharff LB, Alkatib S, Hasdorf S, Schöttler MA, Bock R (2011) Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23:3137–3155. https://doi.org/10.1105/tpc.111.088906
Frailey DC, Chaluvadi SR, Vaughn JN, Coatney CG, Bennetzen JL (2018) Gene loss and genome rearrangement in the plastids of five hemiparasites in the family Orobanchaceae. BMC Plant Biol 18:30. https://doi.org/10.1186/s12870-018-1249-x
Frank G, Hawksworth FG, Wiens D (1996) Dwarf mistletoes: biology, pathology, and systematics. United States Department of Agriculture Forest Service, Washington, DC
Fu CN, Wu CS, Ye LJ, Mo ZQ, Liu J, Chang YW et al (2019) Prevalence of isomeric plastomes and effectiveness of plastome super-barcodes in yews (Taxus) worldwide. Sci Rep-UK 9:2773. https://doi.org/10.1038/s41598-019-39161-x
Funk H, Berg S, Krupinska K, Maier U, 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. https://doi.org/10.1186/1471-2229-7-45
Gilbert JA, Punter D (1990) Release and dispersal of pollen from dwarf mistletoe on jack pine in Manitoba in relation to microclimate. Can J for Res 20:267–273. https://doi.org/10.1139/x90-039
Gilbert JA, Punter D (1991) Germination of pollen of the dwarf mistletoe Arceuthobium americanum. Can J Bot 68:685–688. https://doi.org/10.1139/b91-092
Guo X, Ruan Z (2019a) Characterization of the complete plastome of Dendrophthoe pentandra (Loranthaceae), a stem hemiparasite. Mitochondr DNA B 4:3099–3100. https://doi.org/10.1080/23802359.2019.1667280
Guo X, Ruan Z (2019b) The complete chloroplast genome of Elytranthe albida (Loranthaceae), a hemiparasitic shru. Mitochondr DNA B 4:3112–3113. https://doi.org/10.1080/23802359.2019.1667911
Guo X, Castillo-Ramírez S, González V, Bustos P, Fernández-Vázquez JL, Santamaría RI, Arellano J, Cevallos MA, Dávila G (2007) Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genomics 8:228. https://doi.org/10.1186/1471-2164-8-228
Guo X, Ruan Z, Zhang G (2019) The complete plastome of Taxillus vestitus (Loranthaceae), a hemiparasitic plant. Mitochondr DNA B 4:3188–3189. https://doi.org/10.1080/23802359.2019.1667912
Guo X, Liu C, Zhang G, Su W, Landis JB, Zhang X et al (2020) The Complete plastomes of five hemiparasitic plants (Osyris wightiana, Pyrularia edulis, Santalum album, Viscum liquidambaricolum, and V. ovalifolium): comparative and evolutionary analyses within Santalales. Front Genet 11:597. https://doi.org/10.3389/fgene.2020.00597
Guo X, Liu C, Wang H, Zhang G, Yan H, Jin L, Su W, Ji Y (2021) The complete plastomes of two flowering epiparasites (Phacellaria glomerata and P. compressa): gene content, organization, and plastome degradation. Genomics 113:447–455. https://doi.org/10.1016/j.ygeno.2020.12.031
Hebert PDN, Cywinska A, Ball SL, De-Waard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B 270:313–322. https://doi.org/10.1098/rspb.2002.2218
Hollingsworth PM (2011) Refining the DNA barcode for land plants. Proc Natl Acad Sci USA 108:19451–19452. https://doi.org/10.1073/pnas.1116812108
Hollingsworth PM, Forrest LL, Spouge JL, Hajibabaei M, Ratnasingham S, van der Bank M et al (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797. https://doi.org/10.1073/pnas.0905845106
Hollingsworth PM, Graham SW, Little DP (2011) Choosing and using a plant DNA barcode. PLoS ONE 6:e19254. https://doi.org/10.1371/journal.pone.0019254
Hollingsworth PM, Li DZ, Michelle VDB, Twyford AD (2016) Telling plant species apart with DNA: from barcodes to genomes. Philos Trans R Soc B-Biol Sci 371:20150338. https://doi.org/10.1098/rstb.2015.0338
Horváth EM, Peter SO, Joë T, Rumeau D, Cournac L, Horváth GV, Kavanagh TA, Schäer C, Peltier G, Medgyesy P (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol 123:1337–1350. https://doi.org/10.1104/pp.123.4.1337
Hull RJ, Leonard OA (1964a) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron). I. The carbohydrate nutrition of mistletoe. Am J Bot 39:996–1007. https://doi.org/10.1104/pp.39.6.996
Hull RJ, Leonard OA (1964b) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron). II. The photosynthetic capacity of mistletoe. Am J Bot 39:1008–1017. https://doi.org/10.2307/4260344
Jansen RK, Cai Z, Raubeson LA, Daniell H, de Pamphilis CW, Leebens-Mack J et al (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome–scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374
Ji Y, Liu C, Yang Z, Yang L, He Z, Wang H et al (2019) Testing and using complete plastomes and ribosomal DNA sequences as the next generation DNA barcodes in Panax (Araliaceae). Mol Ecol Resour 19:1333–1345. https://doi.org/10.1111/1755-0998.13050
Ji Y, Liu C, Yang J, Jin L, Yang Z, Yang JB (2020) Ultra-barcoding discovers a cryptic species in Paris yunnanensis (Melanthiaceae), a medicinally important plant. Front Plant Sci 11:411. https://doi.org/10.3389/fpls.2020.00411
Jiang D, Ma R, Li J, Mao Q, Miao N, Mao K (2019) Characterization of the complete chloroplast of Scurrula parasitica. Mitochondr DNA B 4:247–248. https://doi.org/10.1080/23802359.2018.1501294
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kearse M, Richard M, Amy W, Steven SH, Matthew C, Shane S et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kirkpatrick LA (1989) Field study of water relations of dwarf mistletoe and lodgepole pine in central Oregon. Am J Bot 76:111–112
Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121. https://doi.org/10.1007/s00294-008-0208-8
Kress WJ, Wurdack KJ, Zimmer EA et al (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374
Leonard OA, Hull RJ (1965) Translocation relationships in and between mistletoes and their hosts. Hilgardia 37:115–153. https://doi.org/10.3733/hilg.v37n04p115
Li Y, Zhou JG, Chen XL, Cui YX, Xu ZC, Li YH et al (2017) Gene losses and partial deletion of small single–copy regions of the chloroplast genomes of two hemiparasitic Taxillus species. Sci Rep 7:12834. https://doi.org/10.1038/s41598-017-13401-4
Lin CS, Chen JJ, Huang YT, Chan MT, Daniell H, Chang WJ et al (2015) The location and translocation of ndh genes of chloroplast origin in the Orchidaceae family. Sci Rep 5:9040. https://doi.org/10.1038/srep09040
Lin CS, Chen JJ, Chiu CC, Hsiao HC, Yang CJ, Jin XH et al (2017) Concomitant loss of NDH complex–related genes within chloroplast and nuclear genomes in some orchids. Plant J 90:994–1006. https://doi.org/10.1111/tpj.13525
Liu SS, Hu YH, Maghuly F, Porth IM, Mao JF (2018) The complete chloroplast genome sequence annotation for Malania oleifera, a critically endangered and important bioresource tree. Conserv Genet Res 11:271–274. https://doi.org/10.1007/s12686-018-1005-4
Liu X, Fu W, Tang Y, Zhang W, Song Z, Li L et al (2020) Diverse trajectories of plastome degradation in holoparasitic Cistanche and genomic location of the lost plastid genes. J Exp Bot 71:877–892. https://doi.org/10.1093/jxb/erz456
Maier UG, Krupinska K, Berg S, Funk HT, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:1–12. https://doi.org/10.1186/1471-2229-7-45
Mathiasen LM, Shaw DC, Nickrent DL, Watson DM (2008) Mistletoes: pathology, systematics, ecology, and management. Plant Dis 92:988–1006. https://doi.org/10.1094/PDIS-92-7-0988
Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I (2000) VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16:1046–1047
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. https://doi.org/10.1186/1471-2148-8-130
McNeal JR, Kuehl JV, Boore JL, Pamphilis CWD (2007) Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biol 7:57. https://doi.org/10.1186/1471-2229-7-57
Millen RS, Olmstead RG, Adams KL et al (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13:645–658. https://doi.org/10.3732/ajb.0800085
Morais SG, Lopes AS, Gomes PT et al (2021) Genetic and evolutionary analyses of plastomes of the subfamily Cactoideae (Cactaceae) indicate relaxed protein biosynthesis and tRNA import from cytosol. Braz J Bot 44:97–116. https://doi.org/10.1007/s40415-020-00689-2
Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140. https://doi.org/10.1146/annurev.arplant.51.1.111
Ni Z, Ye Y, Bai T, Xu M, Xu LA (2017) Complete chloroplast genome of Pinus massoniana (Pinaceae): gene rearrangements, loss of ndh Genes, and short inverted repeats contraction. Expansion Mol 22:1528. https://doi.org/10.3390/molecules22091528
Nickrent DL (1997) The parasitic plant connection. Available online: http://parasiticplants.siu.edu/. Accessed 7 September 2019
Nickrent DL (2002) Plantas parásitas en el mundo. In: López-Sáez JA, Catalán P, Sáez L (eds) Plantas Parásitas de la Península Ibérica e Islas Baleares. Mundi-Prensa Libros, Madrid, pp 7–27
Nickrent DL, Malécot V, Vidal-Russell R, Der JP (2010) A revised classification of Santalales. Taxon 59:538–558. https://doi.org/10.2307/25677612
Nickrent DL, Anderson F, Kuijt J (2019) Inflorescence evolution in Santalales: integrating morphological characters and molecular phylogenetics. Am J Bot 106:402–414. https://doi.org/10.1002/ajb2.1250
Palmer JD (1985) Comparative organization of chloroplast genomes. Ann Rev Genet 19:325–354. https://doi.org/10.1146/annurev.ge.19.120185.001545
Park S, Jansen RK, Park S (2015) Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae. BMC Plant Biol 15:40. https://doi.org/10.1186/s12870-015-0432-6
Parks CG, Flanagan PT (2001) Dwarf mistletoes (Arceuthobium spp.), rust diseases, and stem decays in eastern Oregon and Washington. Northwest Sci 75:31–337. https://doi.org/10.2307/3858451
Parmeter JR, Scharpf RF (1963) Dwarf mistletoe on red fir and white fir in California. J Forest 61:371–374. https://doi.org/10.1093/jof/61.5.371
Parmeter JR, Hood JR, Scharpf RF (1959) Colletotrichum blight of dwarf mistletoe. Phytopathol 49:812–815
Pel HJ, Grivell LA (1994) Protein synthesis in mitochondria. Mol Biol Rep 165:183–194
Peredo EL, King UM, Les DH (2013) The plastid genome of Najas flexilis: adaptation to submersed environments is accompanied by the complete loss of the NDH complex in an aquatic angiosperm. PLoS ONE 8:e68591. https://doi.org/10.1371/journal.pone.0068591
Petersen G, Cuenca A, Seberg O (2015) Plastome evolution in hemiparasitic mistletoes. Genome Biol Evol 7:2520–2532. https://doi.org/10.1093/gbe/evv165
Qiu HX, Gilbert MG (2003) Viscaceae. In Flora of China, Vol. 5; Z. Y. Wu, P. H. Raven (Eds), pp. 241–242. Beijing, Science Press; aint Louis, Missouri Botanical Garden Press.
Rogalski M, Karcher D, Bock R (2008) Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 15:192–198. https://doi.org/10.1038/nsmb.1370
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:572–1574. https://doi.org/10.1093/bioinformatics/btg180
Ruhsam M, Rai HS, Mathews S, Ross G, Graham SW, Raubeson LA et al (2015) Does complete plastid genome sequencing improve species discrimination and phylogenetic resolution in Araucaria? Mol Ecol Resour 15:1067–1078. https://doi.org/10.1111/1755-0998.12375
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051. https://doi.org/10.1111/j.1365-3040.2007.01675.x
Sabir J, Schwarz EN, Ellison N, Zhang J, Baeshen NA, Mutwakil M, Jansen RK, Ruhlman TA (2014) Evolutionary and biotechnology implications of plastid genome variation in the inverted–repeat lacking clade of legumes. Plant Biotechnol J 12:743–754
Sanderson MJ, Copetti D, Búrquez A, Bustamante E, Charboneau JLM, Eguiarte LE et al (2015) Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): loss of the ndh gene suite and inverted repeat. Am J Bot 102:1115–1127. https://doi.org/10.3732/ajb.1500184
Saski C, Lee S-B, Daniell H, Wood TC, Tomkins J, Kim H-G, Jansen RK (2005) Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol 59:309–322
Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689. https://doi.org/10.1093/nar/gki366
Schneider AC, Chun H, Stefanović S, Baldwin BG (2018) Punctuated plastome reduction and host–parasite horizontal gene transfer in the holoparasitic plant genus Aphyllon. Proc R Soc B 285:20181535. https://doi.org/10.1098/rspb.2018.1535
Schwarz EN, Ruhlman TA, Sabir JS, Hajrah NH, Alharbi NS, Al-Malki AL et al (2015) Plastid genome sequences of legumes reveal parallel inversions and multiple losses of rps16 in papilionoids. J System Evol 53:458–468
Shin HW, Lee NS (2018) Understanding plastome evolution in hemiparasitic Santalales: complete chloroplast genomes of three species, Dendrotrophe varians, Helixanthera parasitica, and Macrosolen cochinchinensis. PLoS ONE 13:e0200293. https://doi.org/10.1371/journal.pone.0200293
Singh P, Carew GE (1989) Impact of eastern dwarf mistletoe in black spruce forests in Newfoundland. Eur J for Pathol 19:305–322. https://doi.org/10.1111/j.1439-0329.1989.tb00266.x
Ślipiko M et al (2020) Molecular delimitation of European leafy liverworts of the genus Calypogeia based on plastid super-barcodes. BMC Plant Biol 20:243. https://doi.org/10.1186/s12870-020-02435-y
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771. https://doi.org/10.1080/10635150802429642
Straub SCK, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364. https://doi.org/10.3732/ajb.1100335
Su HJ, Hu JM (2016) The complete chloroplast genome of hemiparasitic flowering plant Schoepfia jasminodora. Mitochondr DNA B 1:767–769. https://doi.org/10.1080/23802359.2016.1238753
Su HJ, Hu JM, Anderson FE, Nickrent DL (2015) Phylogenetic relationships of Santalales with insights into the origins of holoparasitic Balanophoraceae. Taxon 64:491–506. https://doi.org/10.12705/643.2
Sun Y, Moore MJ, Zhang S, Soltis PS, Soltis DE, Zhao T et al (2016) Phylogenomic and structural analyses of 18 complete plastomes across nearly all families of early–diverging eudicots, including an angiosperm wide analysis of IR gene content evolution. Mol Phylogenet Evol 96:93–101. https://doi.org/10.1016/j.ympev.2015.12.006
Sun Y, Moore MJ, Lin N, Adelalu KF, Meng A, Jian S et al (2017) Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family. BMC Genomics 18:592. https://doi.org/10.1186/s12864-017-3956-3
Tangphatsornruang S, Sangsrakru D, Chanprasert J, Uthaipaisanwong P, Yoocha T, Jomchai N, Tragoonrung S (2010) The chloroplast genome sequence of mungbean (Vigna radiata) determined by high-throughput pyrosequencing: structural organization and phylogenetic relationships. DNA Res 17:11–22. https://doi.org/10.1093/dnares/dsp025
Tocher RD, Gustafson SW, Knutson DM (1984) Water metabolism and seedling photosynthesis in dwarf mistletoes. In: Hawksworth FG, Scharpf F (eds) Biology of dwarf mistletoes, Proceedings of the symposium. Department of Agriculture, Forest Service, Fort Collins, pp 62–69
Tong J, Ren W (1980) Preliminary studies on the disease cycle of Arceuthobium chinense. J Yunnan for Coll 1:19–25
Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiur 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 USA 91:9794–9798. https://doi.org/10.2307/2365708
Wicke S, Naumann J (2018) Molecular evolution of plastid genomes in parasitic flowering plants. Adv Bot Res 85:315–347. https://doi.org/10.1016/bs.abr.2017.11.014
Wicke S, Schneeweiss GM, de Pamphilis CW, Müller KF, Quandt D (2011a) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297
Wicke S, Schneeweiss GM, Depamphilis CW, Kai FM, Quandt D (2011b) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297. https://doi.org/10.1007/s11103-011-9762-4
Wicke S, Müller KF, Depamphilis CW, Quandt D, Wickett NJ, Zhang Y et al (2013) Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell 25:3711–3725. https://doi.org/10.1105/tpc.113.113373
Wicke S, Müller KF, Depamphilis CW, Quandt D, Bellot S, Schneeweiss GM (2016) Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants. Proc Natl Acad Sci USA 113:9045–9050. https://doi.org/10.1073/pnas.1607576113
Wu CS, Lai YT, Lin CP, Wang YN, Chaw SM (2009) Evolution of reduced and compact chloroplast genomes (cpDNAs) in gnetophytes: selection toward a lower–cost strategy. Mol Phylogenet Evol 52:115–124. https://doi.org/10.1016/j.ympev.2008.12.026
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255. https://doi.org/10.1093/bioinformatics/bth352
Yang GS, Wang YH, Shen SK (2017) The complete chloroplast genome of a vulnerable species Champereia manillana (Opiliaceae). Conserv Genet Resour 3:415–418. https://doi.org/10.1007/s12686-017-0697-1
You M (1985) The study of the physiological and biochemical characteristics on the parasitic disease by Arceuthobium chinense Lecomte. J Southwest for Coll 6:8–16
You M, Tong J (1987) Study on biology of Arceuthobium chinense and its harm set to Keteleeria evelyniana. J Southwest for Coll 7:38–46
Yu NJ, Spremulli LL (1998) Regulation of the activity of chloroplast translational initiation factor 3 by NH2- and COOH-terminal extensions. J Biol Chem 165:3871–3877
Zhu ZX, Wang JH, Cai YC, Zhao KK, Moore MJ, Wang HF (2018) Complete plastome sequence of Erythropalum scandens (Erythropalaceae), an edible and medicinally important liana in China. Mitochondr DNA B 3:139–140. https://doi.org/10.1080/23802359.2017.1413435
Acknowledgements
This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK04020103), and the National Natural Science Foundation of China (31060052). We are sincerely grateful to Prof. Wenhua Su for collecting sample of Arceuthobium pini, and to Lei Jin, Jin Yang, Naixing Shi, Li Li and Shuying Wang for their help in data analyses.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
.
Additional information
Communicated by Anastasios Melis.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Guo, X., Zhang, G., Fan, L. et al. Highly degenerate plastomes in two hemiparasitic dwarf mistletoes: Arceuthobium chinense and A. pini (Viscaceae). Planta 253, 125 (2021). https://doi.org/10.1007/s00425-021-03643-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03643-y