Skip to main content
SpringerLink
Log in

Mitochondrial genome sequences reveal evolutionary relationships of the Phytophthora 1c clade species

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Phytophthora infestans is one of the most destructive plant pathogens of potato and tomato globally. The pathogen is closely related to four other Phytophthora species in the 1c clade including P. phaseoli, P. ipomoeae, P. mirabilis and P. andina that are important pathogens of other wild and domesticated hosts. P. andina is an interspecific hybrid between P. infestans and an unknown Phytophthora species. We have sequenced mitochondrial genomes of the sister species of P. infestans and examined the evolutionary relationships within the clade. Phylogenetic analysis indicates that the P. phaseoli mitochondrial lineage is basal within the clade. P. mirabilis and P. ipomoeae are sister lineages and share a common ancestor with the Ic mitochondrial lineage of P. andina. These lineages in turn are sister to the P. infestans and P. andina Ia mitochondrial lineages. The P. andina Ic lineage diverged much earlier than the P. andina Ia mitochondrial lineage and P. infestans. The presence of two mitochondrial lineages in P. andina supports the hybrid nature of this species. The ancestral state of the P. andina Ic lineage in the tree and its occurrence only in the Andean regions of Ecuador, Colombia and Peru suggests that the origin of this species hybrid in nature may occur there.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abad ZG, Abad JA (1997) Another look at the origin of late blight of potatoes, tomatoes and pear melon in the Andes of South America. Plant Dis 81:682–688

    Article  Google Scholar 

  • Adler NE, Chacón G, Forbes G, Flier W (2002) Phytophthora infestans sensu lato in South America population substructuring through host-specificity. In: Lizárrega C (ed) Proceedings of the Global Initiative on Late Blight Conference. International Potato Center, Lima, pp 13–17

    Google Scholar 

  • Adler NE, Erselius LJ, Chacon MG, Flier WG, Ordonez ME, Kroon LPNM, Forbes GA (2004) Genetic diversity of Phytophthora infestans sensu lato in Ecuador provides new insight into the origin of this important plant pathogen. Phytopathology 94:154–162

    Article  CAS  PubMed  Google Scholar 

  • Avila-Adame C, Gómez-Alpizar L, Zisman V, Jones K, Buell CR, Ristaino JB (2006) Mitochondrial genome sequences and molecular evolution of the Irish potato famine pathogen, Phytophthora infestans. Curr Genet 49:39–46

    Article  CAS  PubMed  Google Scholar 

  • Aylor DL, Price EW, Carbone I (2006) SNAP: combine and map modules for multilocus population genetic analysis. Bioinformatics 22:1399–1401

    Article  CAS  PubMed  Google Scholar 

  • Blair JE, Coffey MD, Park S-Y, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Gen Biol 45:266–277

    Article  CAS  Google Scholar 

  • Blair JE, Coffey MD, Martin FN (2012) Species tree estimation for the late blight pathogen, Phytophthora infestans, and close relatives. PLoS One 7:e37003

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bourke PM (1964) Emergence of potato blight. Nature 203:805–808

    Article  Google Scholar 

  • Bowden LC, Price EW, Carbone I (2008) SNAP Clade and Matrix, Version 2. Distributed over the Internet, http://www.cals.ncsu.edu/plantpath/faculty/carbone/home.html. Department of Plant Pathology, North Carolina State University

  • Brasier CM, Hansen EM (1992) Evolutionary biology of Phytophthora. Part II: phylogeny, speciation, and population structure. Ann Rev Phytopathol 30:173–200

    Article  Google Scholar 

  • Carbone I, Liu Y-C, Hillman BI, Milgroom MG (2004) Recombination and migration of Cryphonectria hypovirus I as inferred from gene genealogies and the coalescent analysis. Genetics 166:1611–1629

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cárdenas M, Tabmia J, Fry WE, Grünwald NJ, Bernal A et al (2012) Restrepo SDefining species boundaries in the genus Phytophthora: the case of Phytophthora andina. A response to ‘Phytophthora andina sp. nov., a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands’ (Oliva, 2010). Plant Pathol 61:215–220

    Article  Google Scholar 

  • Carter DA, Archer SA, Buck KW (1990) Restriction fragment length polymorphism of mitochondrial DNA of Phytophthora infestans. Mycol Res 8:1123–1128

    Article  Google Scholar 

  • Chesnick JM, Tuxbury K, Coleman A, Lang BF (1996) Utility of the mitochondrial nad4L gene for algal and protistan phylogenetic analysis. J Phycol 32:452–456

    Article  CAS  Google Scholar 

  • Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Gen Biol 30:17–32

    Article  CAS  Google Scholar 

  • Dong et al (2014) Effector specialization in a lineage of the Irish potato famine pathogen. Science 343:552–555

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed Central  PubMed  Google Scholar 

  • Evans TA, Mulrooney R, Gregory NF, Kee E (2007) Lima bean downy mildew: impact, Etiology, and management strategies for Delaware and the Mid-Atlantic Region. US. Plant Dis. 91:128–135

    Article  Google Scholar 

  • Farr DF, Rossman AY (2014) Fungal Database Systematic Mycology and Microbiology Laboratory. ARS, USDA. http://www.nt.ars-grin.gov/fungaldatabases/

  • Farrer RA et al (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Nat Acad Sci 108:18732–18736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flier WG, Grünwald NJ, Kroon LPNM, van den Bosch TBM, Garay-Serrano E, Lozoya-Saldana Bonants PJM, Turkensteen LJ (2002) Phytophthora ipomoeae sp. nov., a new homothallic species causing leaf blight on Ipomoea longipedunculata in the Toluca Valley of Central Mexico. Mycol Res 106:848–856

    Article  Google Scholar 

  • Flier WG, Grünwald NJ, Kroon LPNM, Sturbaum AK, van den Bosch TBM, Garay-Serrano E, Lozoya-Saldana H, Fry WE, Turkensteen LJ (2003) The population structure of Phytophthora infestans from the Toluca Valley of Central Mexico suggests genetic differentiation between populations of cultivated potato and wild Solanum spp. Phytopathology 93:382–390

    Article  PubMed  Google Scholar 

  • Forbes GA, Ristaino JB, Oliva RF, Flier W (2012) A rebuttal to the letter to the editor concerning “Defining species boundaries in the genus Phytophthora: the case of Phytophthora andina”. Plant Pathol 61:221–223

    Article  Google Scholar 

  • Forbes GA, Morales JG, Restrepo S, Perez S, Gamboa S, Ruiz R, Ceden L, Fermin G, Andreu A, Acuna I, Oliva R (2013) Phytophthora infestans and Phytophthora andina on Solanaceous hosts in South America. In: Lamour K (ed) Phytophthora: a global perspective. CABI International, Oxfordshire, pp 48–58

    Chapter  Google Scholar 

  • Föster H, Coffey MD, Elwood H, Sogin ML (1990) Sequence analysis of the small-subunit ribosomal rRNA’s of three zoosporic fungi and implications for fungal evolution. Mycologia 82:306–312

    Article  Google Scholar 

  • Fry WE, McGrath MT, Seaman A, Zitter TA, McLeod A, Danies G, Small IM, Myers K, Everts K, Gevens AJ, Gugino B, Johnson SB, Judelson H, Ristaino JB, Roberts PB, Secor G, Seebold KW, Snover-Clift KL, Wyenandt A, Grunwald NJ, Smart CD (2013) The 2009 late blight Pandemic in Eastern USA-causes and results. Plant Dis 96:296–306

    Article  Google Scholar 

  • Galindo J, Hohl HR (1985) Phytophthora mirabilis, a new species of Phytophthora. Sydowia 38:87–96

    Google Scholar 

  • Garber RC, Yoder OC (1983) Isolation of DNA from filamentous fungi and separation into nuclear, mitochondrial, ribosomal, and plasmid components. Anal Biochem 135:416–422

    Article  CAS  PubMed  Google Scholar 

  • Gavino PD, Fry WE (2002) Diversity in and evidence for selection of the mitochondrial genome of Phytophthora infestans. Mycologia 94:781–793

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Alpizar L, Carbone I, Ristaino JB (2007) An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene geneologies. Proc Natl Acad Sci 104:3306–3311

    Article  PubMed Central  PubMed  Google Scholar 

  • Gómez-Alpizar L, Hu CH, Oliva RF, Forbes GA, Ristaino JB (2008) Phylogenetic relationships of Phytophthora andina, a new species from the highlands of Ecuador that is closely related to the Irish potato famine pathogen Phytophthora infestans. Mycologia 100:590–602

    Article  PubMed  Google Scholar 

  • Goodwin SB, Fry WE (1994) Genetic analysis of interspecific hybrids between Phytophthora infestans and Phytophthora mirabilis. Exp Mycol 18:20–32

    Article  Google Scholar 

  • Goodwin SB, Cohen BA, Fry WE (1994) Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proc Natl Acad Sci 91:11591–11595

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goodwin SB, Legard DE, Smart CD, Levy M, Fry WE (1999) Gene flow analysis of molecular markers confirms that Phytophthora mirabilis and P. infestans are separate species. Mycologia 91:796–810

    Article  CAS  Google Scholar 

  • Goss EM, Cardenas ME, Myers K, Forbes G, Fry WE, Restrepo S, Grünwald N (2011) The plant pathogen Phytophthora andina emerged via hybridization of an unknown Phytophthora species and the Irish potato famine pathogen P. infestans. PLos One 6:e24543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goss EM, Tabima JF, Cooke DE, Restrepo S, Fry WE, Forbes GA, Fieland V, Cardenas M, Grünwald NJ (2014) The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proc Natl Acad Sci 24:8791–8796

    Article  Google Scholar 

  • Griffith GW, Shaw DS (1998) Polymorphisms in Phytophthora infestans: four mitochondrial haplotypes are detected after PCR amplification of DNA from pure cultures or from host lesions. Appl Envir Microbiol 64:4007–4014

    CAS  Google Scholar 

  • Griffiths RC, Tavaré S (1994) Ancestral inference in population genetics. Stat Sci 9:307–319

    Article  Google Scholar 

  • Grünwald NJ, Flier WG (2005) The biology of Phytophthora infestans at its center of origin. Ann Rev Phytopathol 43:171–190

    Article  Google Scholar 

  • Gunderson JH, Elwood H, Ingold A, Kindle K, Soin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci 84:5823–5827

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 41:95–98

    CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Ecol 22:160–174

    Article  CAS  Google Scholar 

  • Hawkes JG (1990) The potato: evolution, biodiversity and genetics resources. Belhaven Press, London

    Google Scholar 

  • Hu CH, Perez FG, Donahoo R, McLeod A, Myers K, Ivors K, Secor G, Roberts PD, Fry WE, Deahl KL, Ristaino JB (2012) Recent genotypes of Phytophthora infestans in eastern USA reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Dis 96:1323–1330

    Article  Google Scholar 

  • Klimczak LJ, Prell HH (1984) Isolation and characterization of mitochondrial DNA of the oomycete fungus Phytophthora infestans. Curr Genet 8:323–326

    Article  CAS  PubMed  Google Scholar 

  • Kroon LPNM, Bakker FT, van den Bosch BGM, Bonants PJM, Flier WG (2004) Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet Biol 41:766–782

    Article  CAS  PubMed  Google Scholar 

  • Lang BF, Forget L (1993) The mitochondrial genome of Phytophthora infestans. In: O’Brien SJ (ed) Genetic maps: locus maps of complex genomes. Cold Spring Harbor Laboratory Press, Plan View, pp 3.133–3.135

  • Lassiter ES, Russ C, Nusbaum C, Zeng Q, Hu CH, Thorne JL, Ristaino JB (2010) Inferring evolutionary relationships of species in the Phytophthora 1c clade using nuclear and mitochondrial genes. Phytopathology 100:S68

    Google Scholar 

  • Lennon NJ et al (2010) A scalable, fully automated process for construction of sequence-ready barcoded libraries for 454. Genome Biol 11:R15

    Article  PubMed Central  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed Central  PubMed  Google Scholar 

  • Lindgreen S (2012) AdapterRemoval: easy cleaning of next-generation sequencing reads. BMC Res Notes 5:337

    Article  PubMed Central  PubMed  Google Scholar 

  • Martin MD et al (2013) Reconstructing genome evolution in historic samples of the Irish potato famine pathogen. Nat Commun 4:2172. doi:10.1038/ncomms3172

    PubMed Central  PubMed  Google Scholar 

  • Martin MD, Ho SY, Wales N, Ristaino JB, Gilbert MTP (2014) Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant New World Phytophthora infestans. Mol Biol Evol 31:1416–1420

    Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oliva RF, Kroon LPNM, Chacón G, Flier WG, Ristaino JB, Forbes GA (2010) Phytophthora andina sp. nov., a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands. Plant Path 100:590–602

    Google Scholar 

  • Ordonez ME, Hohl HR, Velasco JA, Ramon MP, Oyarzun PJ, Smart CD, Fry WE, Forbes GA, Erselius LJ (2000) A novel population of Phytophthora, similar to Phytophthora infestans, attacks wild Solanum species in Ecuador. Ecol Pop Biol 90:197–202

    CAS  Google Scholar 

  • Paquin B, Laforest M-J, Forget L, Roewer I, Wang Z, Longcore J, Lang BF (1997) The fungal mitochondrial genome project:evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 31:380–395

    Article  CAS  PubMed  Google Scholar 

  • Price EW, Carbone I (2005) SNAP: workbench management tool for evolutionary population genetic analysis. Bioinformatics 21:402–404

    Article  CAS  PubMed  Google Scholar 

  • Raffaele S et al (2010) Genome evolution following host jumps in the Irish potato famine lineage. Science 330:1540–1543

    Article  CAS  PubMed  Google Scholar 

  • Rambaut A (2007) FigTree. Mol Evol Phylogenet Epidemiol. http://www.tree.bio.ed.ac.uk/software/figtree/

  • Ristaino JB, Groves CT, Parra GR (2001) PCR amplification of the Irish potato famine pathogen from historic specimens. Nature 411:695–697

    Article  CAS  PubMed  Google Scholar 

  • Robideau GP, de Cock AWAM, Coffey MD, Voglmayr H, Bonants PJM, Ristaino JB, Chitty D, Rintoul T, Désaulniers N, Eggertson Q, Bala K, Gachon CMM, Smith ML, Lévesque A (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit I (COI). Mol Ecol Res 11:1002–1011

    Article  CAS  Google Scholar 

  • Thaxter R (1889) A new American Phytophthora. Bot Gaz 14:273–274

    Article  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetic models without recombination. Theor Pop Biol 7:256–276

    Article  CAS  Google Scholar 

  • Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, Thines M, Weigel D, Burbano HA (2013) The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2:e00731

    PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

A graduate teaching assistantship from the Department of Genetics at NC State University funded Erica Lassiter’s work. The senior author is now employed at Bayer Crop Science RTP, NC. Some of the research (J.L. Thorne) was partially supported by NIH Grant GM070806 and supplies were funded by USDA NIFA Grant #2006-55319-16550 and Agriculture and Food Research Initiative Competitive Grants Program (AFRI) Grant 2011-68004-30154. The Copenhagen-based sequencing was funded by Lundbeck Foundation Grant R52-5062 and appreciation is expressed to Tom Gilbert’s laboratory for sequencing the Ia lineage of P. andina. Appreciation for providing cultures is expressed to: Gregory Forbes and Ricardo Oliva International Potato Center (Oliva now at the International Rice Research Institute, Philippines) for P. andina; Peter Bonants, Plant Research International, Wageningen for P. ipomoeae; Mike Coffey, University of California Riverside for P. mirabilis; and Tom Evans and Nancy Gregory, University of Delaware, for P. phaseoli used in this work. The technical support of Dr. Julia Hu, Dr. Monica Blanco Menenses and Caleb Pearce is appreciated. Dr. Geromy Moore, Dr. Ben Redelings, Dr. Reed Cartwright and Kristin Lamm helped troubleshoot analytical methods and simulations.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, North Carolina State University, Raleigh, NC, 27695, USA

    Erica S. Lassiter

  2. BROAD Institute, MIT, Cambridge, MA, 02142, USA

    Carsten Russ, Chad Nusbaum & Qiandong Zeng

  3. Department of Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA

    Amanda C. Saville, Rodrigo A. Olarte, Ignazio Carbone, Chia-Hui Hu & Jean B. Ristaino

  4. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

    Andaine Seguin-Orlando & Jose A. Samaniego

  5. Department of Biological Sciences and Department of Statistics, North Carolina State University, Raleigh, NC 27695, USA

    Jeffrey L. Thorne

Authors
  1. Erica S. Lassiter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carsten Russ
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chad Nusbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiandong Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amanda C. Saville
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rodrigo A. Olarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ignazio Carbone
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chia-Hui Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Andaine Seguin-Orlando
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jose A. Samaniego
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jeffrey L. Thorne
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jean B. Ristaino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean B. Ristaino.

Additional information

Communicated by L. Tomaska.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 87 kb)

Supplementary material 2 (DOCX 158 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lassiter, E.S., Russ, C., Nusbaum, C. et al. Mitochondrial genome sequences reveal evolutionary relationships of the Phytophthora 1c clade species. Curr Genet 61, 567–577 (2015). https://doi.org/10.1007/s00294-015-0480-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0480-3

Keywords

Search

Navigation