Molecular Breeding

, 36:116 | Cite as

Toward the elucidation of cytoplasmic diversity in North American grape breeding programs

  • Jonathan Fresnedo-Ramírez
  • Qi Sun
  • Chin-Feng Hwang
  • Craig A. Ledbetter
  • David W. Ramming
  • Anne Y. Fennell
  • M. Andrew Walker
  • James J. Luby
  • Matthew D. Clark
  • Jason P. Londo
  • Lance Cadle-Davidson
  • Gan-Yuan Zhong
  • Bruce I. Reisch
Short Communication
  • 368 Downloads

Abstract

Plants have an intriguing tripartite genetic system: Nuclear genome × Mitochondria × Plastids and their interactions may impact germplasm breeding. In grapevine, the study of cytoplasmic genomes has been limited, and their role with respect to grapevine germplasm diversity has yet to be elucidated. In the present study, the results of an analysis of the cytoplasmic diversity among 6073 individuals (comprising cultivars, interspecific hybrids and segregating progenies) are presented. Genotyping by sequencing (GBS) was used to elucidate plastid and mitochondrial DNA sequences, and results were analyzed using multivariate techniques. Single nucleotide polymorphism (SNP) effects were annotated in reference to plastid and mitochondrial genome sequences. The cytoplasmic diversity identified was structured according to synthetic domestication groups (wine and raisin/table grape types) and interspecific-hybridization-driven groups with introgression from North American Vitis species, identifying five cytoplasmic groups and four major clusters. Fifty-two SNP markers were used to describe the diversity of the germplasm. Ten organelle genes showed distinct SNP annotations and effect predictions, of which six were chloroplast-derived and three were mitochondrial genes, in addition to one mitochondrial SNP affecting a nonannotated open reading frame. The results suggest that the application of GBS will aid in the study of cytoplasmic genomes in grapevine, which will enable further studies on the role of cytoplasmic genomes in grapevine germplasm, and then allow the exploitation of these sources of diversity in breeding.

Keywords

Plastid genome Mitochondria genome Cytoplasmic differentiation Cytoplasmic lineage Organelle genes Vitis Grapevine 

References

  1. Adam-Blondon A, Jaillon O, Vezzulli S, Zharkikh A, Troggio M, Velasco R (2011) Genome sequence initiatives. In: Adam-Blondon A-Fo, Martínez-Zapater JM, Kole C (eds) Genetics, genomics and breeding of crop plants. Science Publishers, Enfield, pp 211–234Google Scholar
  2. Arroyo-García R, Lefort F, de Andrés MT, Ibañez J, Borrego J, Jouve N, Cabello F, Martínez-Zapater JM (2002) Chloroplast microsatellite polymorphisms in Vitis species. Genome 45(6):1142–1149CrossRefPubMedGoogle Scholar
  3. Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155(4):1520–1532CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bouvier F, Mialoundama AS, Camara B (2009) A sentinel role for plastids. In: Sandelius A, Aronsson H (eds) The chloroplast, vol 13. Plant cell monographs. Springer Berlin, pp 267–292Google Scholar
  5. Chung S-M, Gordon VS, Staub JE (2007) Sequencing cucumber (Cucumis sativus L.) chloroplast genomes identifies differences between chilling-tolerant and -susceptible cucumber lines. Genome 50(2):215–225CrossRefPubMedGoogle Scholar
  6. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu XY, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w(1118); iso-2; iso-3. Fly 6(2):80–92CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cingolani P, Cunningham F, McLaren W, Wang K (2015) Variant annotations in VCF format version 1.0. Available on-line http://snpeff.sourceforge.net/VCFannotationformat_v1.0.pdf
  8. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, Genomes Project Analysis G (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158CrossRefPubMedPubMedCentralGoogle Scholar
  9. Eckardt NA (2006) Cytoplasmic male sterility and fertility restoration. Plant Cell 18(3):515–517CrossRefPubMedCentralGoogle Scholar
  10. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9(2):e90346CrossRefPubMedPubMedCentralGoogle Scholar
  11. Goremykin VV, Salamini F, Velasco R, Viola R (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26(1):99–110CrossRefPubMedGoogle Scholar
  12. Hedrick UP, Booth NO, Dorsey MJ, Taylor OM, Wellington R (1908) The grapes of New York, Report of the New York Agricultural Experiment Station for the year 1907. JB Lyon Company, AlbanyGoogle Scholar
  13. Hyma KE, Barba P, Wang M, Londo JP, Acharya CB, Mitchell SE, Sun Q, Reisch B, Cadle-Davidson L (2015) Heterozygous Mapping Strategy (HetMappS) for high resolution genotyping-by-sequencing markers: a case study in grapevine. PLoS ONE 10(8):e0134880CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P, French-Italian Public Consortium for Grapevine Genome C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467CrossRefPubMedGoogle Scholar
  15. Janeiro P, Brett AMO (2007) Redox behavior of anthocyanins present in Vitis vinifera L. Electroanal 19(17):1779–1786CrossRefGoogle Scholar
  16. Jansen RK, Kaittanis C, Saski C, Lee SB, Tomkins J, Alverson AJ, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32. doi:10.1186/1471-2148-6-32 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kupsch C, Ruwe H, Gusewski S, Tillich M, Small I, Schmitz-Linneweber C (2012) Arabidopsis chloroplast RNA binding proteins CP31A and CP29A associate with large transcript pools and confer cold stress tolerance by influencing multiple chloroplast RNA processing steps. Plant Cell 24(10):4266–4280CrossRefPubMedPubMedCentralGoogle Scholar
  18. Li J, Hu L, Zhang L, Pan X, Hu X (2015) Exogenous spermidine is enhancing tomato tolerance to salinity–alkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. BMC Plant Biol 15(1):1–17CrossRefGoogle Scholar
  19. Liang Z, Yang C, Yang J, Wu B, Wang L, Cheng J, Li S (2009) Inheritance of anthocyanins in berries of Vitis vinifera grapes. Euphytica 167(1):113–125CrossRefGoogle Scholar
  20. Lopez JV, Yuhki N, Masuda R, Modi W, Obrien SJ (1994) Numt, a recent transfer and tandem amplification of mitochondrial-DNA to the nuclear genome of the domestic cat. J Mol Evol 39(2):174–190PubMedGoogle Scholar
  21. Lózsa R, Xia N, Deak T, Bisztray GD (2015) Chloroplast diversity indicates two independent maternal lineages in cultivated grapevine (Vitis vinifera L. subsp vinifera). Genet Resour Crop Evol 62(3):419–429. doi:10.1007/s10722-014-0169-3
  22. Mandel JR, McCauley DE (2015) Pervasive mitochondrial sequence heteroplasmy in natural populations of wild carrot, Daucus carota spp. carota L. PLoS ONE 10(8):e0136303CrossRefPubMedPubMedCentralGoogle Scholar
  23. Mandel JR, McAssey EV, Roland KM, McCauley DE (2012) Mitochondrial gene diversity associated with the atp9 stop codon in natural populations of wild carrot (Daucus carota ssp. carota). J Hered 103(3):418–425CrossRefPubMedGoogle Scholar
  24. Marechal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186(2):299–317CrossRefPubMedGoogle Scholar
  25. Mower J, Sloan D, Alverson A (2012) Plant mitochondrial genome diversity: the genomics revolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ (eds) Plant genome diversity, vol 1. Springer, Vienna, pp 123–144CrossRefGoogle Scholar
  26. Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia JM, Ware D, Bustamante CD, Buckler ES (2011) Genetic structure and domestication history of the grape. Proc Natl Acad Sci U S A 108(9):3530–3535CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nie S, Yue H, Zhou J, Xing D (2015) Mitochondrial-derived reactive oxygen species play a vital role in the salicylic acid signaling pathway in Arabidopsis thaliana. PLoS ONE 10(3):e0119853CrossRefPubMedPubMedCentralGoogle Scholar
  28. Picardi E, Horner DS, Chiara M, Schiavon R, Valle G, Pesole G (2010) Large-scale detection and analysis of RNA editing in grape mtDNA by RNA deep-sequencing. Nucleic Acids Res 38(14):4755–4767CrossRefPubMedPubMedCentralGoogle Scholar
  29. R development core team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  30. Rousseau-Gueutin M, Ayliffe MA, Timmis JN (2011) Conservation of plastid sequences in the plant nuclear genome for millions of years facilitates endosymbiotic evolution. Plant Physiol 157(4):2181–2193CrossRefPubMedPubMedCentralGoogle Scholar
  31. Sanetomo R, Gebhardt C (2015) Cytoplasmic genome types of European potatoes and their effects on complex agronomic traits. BMC Plant Biol 15:162CrossRefPubMedPubMedCentralGoogle Scholar
  32. Sloan DB (2013) One ring to rule them all? Genome sequencing provides new insights into the ‘master circle’ model of plant mitochondrial DNA structure. New Phytol 200(4):978–985CrossRefPubMedGoogle Scholar
  33. Strefeler MS, Weeden NF, Reisch BI (1992) Inheritance of chloroplast DNA in two full-sib Vitis populations. Vitis 31(4):183–187Google Scholar
  34. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22(12):1540–1542CrossRefPubMedGoogle Scholar
  35. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135CrossRefPubMedGoogle Scholar
  36. Tomkins JP, Peterson DG, Yang TJ, Main D, Ablett EF, Henry RJ, Lee LS, Holton TA, Waters D, Wing RA (2001) Grape (Vitis vinifera L.) BAC library construction, preliminary STC analysis, and identification of clones associated with flavonoid and stilbene biosynthesis. Am J Enol Viticult 52(4):287–291Google Scholar
  37. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2(12):e1326CrossRefPubMedPubMedCentralGoogle Scholar
  38. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370CrossRefGoogle Scholar
  39. Westhoff P, Alt J, Herrmann RG (1983) Localization of the genes for the two chlorophyll a-conjugated polypeptides (mol. wt. 51 and 44 kd) of the photosystem II reaction center on the spinach plastid chromosome. EMBO J 2(12):2229–2237PubMedPubMedCentralGoogle Scholar
  40. Woloszynska M (2010) Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes—though this be madness, yet there’s method in’t. J Exp Bot 61(3):657–671CrossRefPubMedGoogle Scholar
  41. Wu J, Krutovskii KV, Strauss SH (1998) Abundant mitochondrial genome diversity, population differentiation and convergent evolution in pines. Genetics 150(4):1605–1614PubMedPubMedCentralGoogle Scholar
  42. Yang S, Fresnedo-Ramírez J, Wang M, Cote L, Schweitzer P, Barba P, Takacs EM, Clark MD, Luby JJ, Manns DC, Sacks GL, Mansfield AK, Londo JP, Fennell AY, Gadoury D, Reisch BI, Cadle-Davidson LE, Sun Q (2016) A next-generation marker genotyping platform (AmpSeq) in heterozygous crops: a case study for marker assisted selection in grapevine. Horticult Res 3:16002CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2016

Authors and Affiliations

  • Jonathan Fresnedo-Ramírez
    • 1
    • 10
  • Qi Sun
    • 1
  • Chin-Feng Hwang
    • 2
  • Craig A. Ledbetter
    • 3
  • David W. Ramming
    • 3
    • 9
  • Anne Y. Fennell
    • 4
  • M. Andrew Walker
    • 5
  • James J. Luby
    • 6
  • Matthew D. Clark
    • 6
  • Jason P. Londo
    • 7
  • Lance Cadle-Davidson
    • 7
  • Gan-Yuan Zhong
    • 7
  • Bruce I. Reisch
    • 8
  1. 1.BRC Bioinformatics Facility, Institute of BiotechnologyCornell UniversityIthacaUSA
  2. 2.State Fruit Experiment Station at Mountain Grove Campus, Darr School of AgricultureMissouri State UniversitySpringfieldUSA
  3. 3.USDA-ARS San Joaquin Valley Agricultural Sciences CenterParlierUSA
  4. 4.Department of Plant ScienceSouth Dakota State UniversityBrookingsUSA
  5. 5.Department of Viticulture and EnologyUniversity of CaliforniaDavisUSA
  6. 6.Department of Horticultural ScienceUniversity of MinnesotaSt. PaulUSA
  7. 7.USDA-ARS Grape Genetics Research UnitGenevaUSA
  8. 8.Horticulture Section, School of Integrative Plant ScienceCornell UniversityGenevaUSA
  9. 9.Ramming’s Specialty CropsFresnoUSA
  10. 10.Department of Horticulture and Crop ScienceThe Ohio State University/OARDCWoosterUSA

Personalised recommendations