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Genome of Irish Potato Famine Pathogen Decoded

11.09.2009
A large international research team has decoded the genome of the notorious organism that triggered the Irish potato famine in the mid-19th century and now threatens this season’s tomato and potato crops across much of the US.

Published in the September 9 online issue of the journal Nature, the study reveals that the organism boasts an unusually large genome size — more than twice that of closely related species — and an extraordinary genome structure, which together appear to enable the rapid evolution of genes, particularly those involved in plant infection. These data expose an unusual mechanism that enables the pathogen to outsmart its plant hosts and may help researchers unlock new ways to control it.

“This pathogen has an exquisite ability to adapt and change, and that’s what makes it so dangerous,” said senior author Chad Nusbaum, co-director of the Genome Sequencing and Analysis Program at the Broad Institute of MIT and Harvard. “We now have a comprehensive view of its genome, revealing the unusual properties that drive its remarkable adaptability. Hopefully, this knowledge can foster novel approaches to diagnose and respond to outbreaks.”

“Our findings suggest a ‘two-speed’ genome, meaning that different parts of the genome are evolving at different rates,” said co-lead author Sophien Kamoun, head of the Sainsbury Laboratory in Norwich, UK. “Future sequencing of additional strains and close relatives of this pathogen will help test this hypothesis and could transform our understanding of how it adapts to immune plants."

The potato famine that gripped Europe, particularly Ireland, in the mid 1800’s was the work of an insidious organism known as Phytophthora infestans. Long considered a fungus, it is now known to be a member of the oomycetes or “water molds,” which are more closely related to the malaria parasite than to fungi. P. infestans thrives in cool, wet weather, and can infect potatoes, tomatoes and other related plants, causing a “late blight” disease that can decimate entire fields in just a few days.

Not only swift in its destruction, the pathogen is also remarkable in its ability to change. For example, it can quickly adapt to new plant hosts, attacking even genetically resistant potatoes that have been painstakingly bred to fend off P. infestans infection. How the pathogen can adapt so rapidly to these immune potatoes has long puzzled scientists.

To understand the genetic basis for the pathogen’s adaptive success, the researchers, led by scientists at the Broad Institute and the Sainsbury Laboratory, decoded the P. infestans genome. They produced a high-quality genome sequence and compared it to the genomes of two relatives: P. sojae, which infects soybeans, and P. ramorum, which prefers oak and other trees and causes a condition known as sudden oak death.

One of the most striking findings to emerge from these comparisons is the expanded nature of the P. infestans genetic blueprint: It is two and a half to four times the size of its relatives’ genomes.

But perhaps even more surprising than the genome’s large size is the source of its added bulk. Nusbaum and his colleagues determined that the additional genomic real estate does not reflect more genes per se, but instead stems from a massive expansion in the amount of repetitive (once considered to be “junk”) DNA. In fact, this type of DNA accounts for about 75% of the entire P. infestans genome.

“Such a large amount of repetitive DNA is pretty surprising, since there is a metabolic cost to maintain it,” said Nusbaum. “As a genome biologist, I have to wonder how the organism benefits from having it.”

The researchers gained some key insights into the potential advantages of carrying this glut of repetitive DNA by probing its genomic structure. They made three critical observations:

• The P. infestans genome comprises alternating repeat-rich (and gene-poor) regions and gene-dense regions;
• These gene-dense regions are shared among other Phytophthora species, preserved over millions of years of evolution, whereas the repeat-rich regions are undergoing relatively rapid changes;

• The repeat-rich regions contain fewer genes compared to other genomic regions, yet those genes they do contain are enriched for those that play crucial roles in plant infection.

Taken together, these findings suggest an unusual genomic strategy to support the rapid evolution of critical genes, known as “effector” genes. Effector genes can disrupt plants’ normal physiology, enabling the pathogen to establish a foothold. However, some can also trigger plants’ immune responses, making them prime targets for combating P. infestans infection.

“We think this could be a tactic that enables P. infestans to rapidly adapt to host plants,” said co-lead author Brian Haas, manager of genome annotation, outreach, bioinformatics, and analysis at the Broad Institute. “In contrast to the well-conserved regions where most genes are found, the repeat-rich regions change rapidly over time, acting as a kind of incubator to enable the rapid birth and death of genes that are key to plant infection. As a result, these critical genes may be gained and lost so rapidly that the hosts simply can’t keep up.”

Importantly, the new P. infestans genome sequence enabled the researchers to identify many previously unknown effector genes, particularly those that belong to two key groups, known as RXLR genes and CRN genes. The research team identified more than 500 RXLR genes and nearly 200 CRN genes, significantly more than are found in the pathogen’s relatives.

These findings not only expand the catalog of known P. infestans genes, they also highlight a critical subset of genes undergoing rapid turnover. Further studies of these genes will foster a deeper understanding of plant infection and help identify potential targets for fighting back.

Paper cited:

Haas et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature DOI:10.1038/nature08358

A complete list of the study’s authors and their affiliations:

Brian J. Haas1,*, Sophien Kamoun2,3,*, Michael C. Zody1,4, Rays H.Y. Jiang1,5, Robert E. Handsaker1, Liliana M. Cano2, Manfred Grabherr1, Chinnappa D. Kodira1†, Sylvain Raffaele2, Trudy Torto-Alalibo3†, Tolga O. Bozkurt2, Audrey M.V. Ah-Fong6, Lucia Alvarado1, Vicky L. Anderson7, Miles R. Armstrong8, Anna Avrova8, Laura Baxter9, Jim Beynon9, Petra C. Boevink8, Stephanie R. Bollmann10, Jorunn I.B. Bos3, Broad Institute Genome Sequencing Platform1, Vincent Bulone11, Guohong Cai12, Cahid Cakir3, James C. Carrington13, Megan Chawner14, Lucio Conti15, Stefano Costanzo16, Richard Ewan15, Noah Fahlgren13, Michael A. Fischbach17, Johanna Fugelstad11, Eleanor M. Gilroy8, Sante Gnerre1, Pamela J. Green18, Laura J. Grenville-Briggs7, John Griffith14, Niklaus J. Grünwald10, Karolyn Horn14, Neil R. Horner7, Chia-Hui Hu19, Edgar Huitema3, Dong- Hoon Jeong18, Alexandra M.E. Jones2, Jonathan D.G. Jones2, Richard W. Jones20, Elinor K. Karlsson1, Sridhara G. Kunjeti21, Kurt Lamour 22, Zhenyu Liu 3, LiJun Ma 1, Daniel MacLean 2, Marcus C. Chibucos23, Hayes McDonald24, Jessica McWalters14, Harold J.G. Meijer5, William Morgan25, Paul F. Morris26, Carol A. Munro27, Keith O'Neill1†, Manuel Ospina-Giraldo14, Andrés Pinzón28, Leighton Pritchard8, Bernard Ramsahoye29, Qinghu Ren30, Silvia Restrepo28, Sourav Roy6, Ari Sadanandom15, Alon Savidor31, Sebastian Schornack2, David C. Schwartz32, Ulrike D. Schumann7, Ben Schwessinger2, Lauren Seyer14, Ted Sharpe1, Cristina Silvar2, Jing Song3, David J. Studholme2, Sean Sykes1, Marco Thines2, 33, Peter J.I. van de Vondervoort5, Vipaporn Phuntumart26, Stephan Wawra7, Rob Weide5, Joe Win2, Carolyn Young3, Shiguo Zhou32, William Fry12, Blake C. Meyers18, Pieter van West7, Jean Ristaino19, Francine Govers5, Paul R. J. Birch34, Stephen C. Whisson8, Howard S. Judelson6, Chad Nusbaum1

*These authors contributed equally to this work

1 Broad Institute of MIT and Harvard, Cambridge MA 02141, USA
2 The Sainsbury Laboratory, Norwich NR4 7UK, UK
3 Department of Plant Pathology, The Ohio State University, Ohio Agricultural Research
and Development Center, Wooster OH 44691, USA
4 Department of Medical Biochemistry and Microbiology, Uppsala University, Box 597,
Uppsala SE-751 24, Sweden
5 Laboratory of Phytopathology, Wageningen University, Wageningen 5-6709 PD, The
Netherlands
6 Department of Plant Pathology and Microbiology, University of California, Riverside
CA 92521, USA
7 University of Aberdeen, Aberdeen Oomycete Group, College of Life Sciences and
Medicine, Institute of Medical Sciences, Foresterhill, Aberdeen AB25 2ZD, UK
8 Plant Pathology Programme, Scottish Crop Research Institute, Invergowrie, Dundee
DD2 5DA, UK
9 University of Warwick, Wellesbourne, Warwick CV35 9EF, UK
10 Horticultural Crops Research Laboratory, USDA Agricultural Research Service,
Corvallis OR 97330, USA
11 Royal Institute of Technology (KTH), School of Biotechnology, AlbaNova University
Centre, Stockholm SE-10691, Sweden
12 Department of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca
NY 14853, USA
13 Center for Genome Research and Biocomputing and Department of Botany and Plant
Pathology, Oregon State University, Corvallis OR 97331, USA
14 Biology Department, Lafayette College, Easton PA 18042, USA
15 Institute of Biomedical and Life Sciences, Bower Building, University of Glasgow,
Glasgow G12 8QQ, UK
16 USDA-ARS, Dale Bumpers National Rice Research Center, Stuttgart AR 72160, USA
17 Department of Molecular Biology, Massachusetts General Hospital, Boston, MA
02114, mfischbach@partners.org, Ph: 617-643-6251
18 Delaware Biotechology Institute, University of Delaware, Newark DE 19711, USA
19 Department of Plant Pathology, North Carolina State University, Raleigh NC 27695,
USA
20 USDA-ARS, Beltsville MD 20705, USA
21 Department of Plant and Soil Sciences, University of Delaware, Newark DE 19711,
USA
22 Entomology and Plant Pathology Department, University of Tennessee, Knoxville TN
37996, USA
23 Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore
MD 21201, USA
24 Dept of Biochemistry, Vanderbilt University School of Medicine, Nashville TN
37203, USA
25 The College of Wooster, Department of Biology, Wooster OH 44691, USA
26 Department of Biological Sciences, Bowling Green State University, Bowling Green
OH 43403, USA
27 University of Aberdeen, School of Medical Sciences, College of Life Sciences and
Medicine, Institute of Medical Sciences, Foresterhill, Aberdeen AB25 2ZD, UK
28 Mycology and Phytopathology Laboratory, Los Andes University, Bogotá, Colombia
29 Institute of Genetics and Molecular Medicine, University of Edinburgh, Cancer
Research Centre, Western General Hospital, Edinburgh EH4 2XU, UK
30 J. Craig Venter Institute, Rockville MD 20850, USA
31 Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel
32 Department of Chemistry, Laboratory of Genetics, Laboratory for Molecular and
Computational Genomics, University of Wisconsin Biotechnology Center, University of
Wisconsin-Madison, Madison WI 53706, USA
33 University of Hohenheim, Institute of Botany 210, D-70593 Stuttgart, Germany
34 Division of Plant Science, College of Life Sciences, University of Dundee (at SCRI),

Invergowrie, Dundee DD2 5DA, UK

About the Broad Institute of MIT and Harvard
The Eli and Edythe L. Broad Institute of MIT and Harvard was founded in 2003 to empower this generation of creative scientists to transform medicine with new genome-based knowledge. The Broad Institute seeks to describe all the molecular components of life and their connections; discover the molecular basis of major human diseases; develop effective new approaches to diagnostics and therapeutics; and disseminate discoveries, tools, methods and data openly to the entire scientific community.

Founded by MIT, Harvard and its affiliated hospitals, and the visionary Los Angeles philanthropists Eli and Edythe L. Broad, the Broad Institute includes faculty, professional staff and students from throughout the MIT and Harvard biomedical research communities and beyond, with collaborations spanning over a hundred private and public institutions in more than 40 countries worldwide. For further information about the Broad Institute, go to www.broadinstitute.org.

About the Sainsbury Laboratory
The Sainsbury Laboratory (TSL) is a world-leading research centre focusing on making fundamental discoveries about plants and how they interact with microbes. TSL is evolving its scientific mission so that it not only provides fundamental biological insights into plant-pathogen interactions, but also delivers novel, genomics-based solutions, which will significantly reduce losses from major diseases of food crops, especially in developing countries. For further information about the Sainsbury Laboratory, go to www.tsl.ac.uk.

Nicole M. Davis | Newswise Science News
Further information:
http://www.bbsrc.ac.uk
http://www.broadinstitute.org

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