Genomics of gene banks: A case study in rice.

Only a small fraction of the naturally occurring genetic diversity available in the world's germplasm repositories has been explored to date, but this is expected to change with the advent of affordable, high-throughput genotyping and sequencing technology. It is now possible to examine genome-wide patterns of natural variation and link sequence polymorphisms with downstream phenotypic consequences. In this paper, we discuss how dramatic changes in the cost and efficiency of sequencing and genotyping are revolutionizing the way gene bank scientists approach the responsibilities of their job. Sequencing technology provides a set of tools that can be used to enhance the quality, efficiency, and cost-effectiveness of gene bank operations, the depth of scientific knowledge of gene bank holdings, and the level of public interest in natural variation. As a result, gene banks have the chance to take on new life. Previously seen as "warehouses" where seeds were diligently maintained, but evolutionarily frozen in time, gene banks could transform into vibrant research centers that actively investigate the genetic potential of their holdings. In this paper, we will discuss how genotyping and sequencing can be integrated into the activities of a modern gene bank to revolutionize the way scientists document the genetic identity of their accessions; track seed lots, varieties, and alleles; identify duplicates; and rationalize active collections, and how the availability of genomics data are likely to motivate innovative collaborations with the larger research and breeding communities to engage in systematic and rigorous phenotyping and multilocation evaluation of the genetic resources in gene banks around the world. The objective is to understand and eventually predict how variation at the DNA level helps determine the phenotypic potential of an individual or population. Leadership and vision are needed to coordinate the characterization of collections and to integrate genotypic and phenotypic information in ways that will illuminate the value of these resources. Genotyping of collections represents a powerful starting point that will enable gene banks to become more effective as stewards of crop biodiversity.

[1]  E. Septiningsih,et al.  Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon , 2003, Theoretical and Applied Genetics.

[2]  C. Bustamante,et al.  Evolutionary History of GS3, a Gene Conferring Grain Length in Rice , 2009, Genetics.

[3]  G. Atlin,et al.  A large-effect QTL for rice grain yield under upland drought stress on chromosome 1 , 2011, Molecular breeding.

[4]  D. Balding,et al.  Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome , 2010, Proceedings of the National Academy of Sciences.

[5]  P. Moncada,et al.  Quantitative trait loci for yield and yield components in an Oryza sativa×Oryza rufipogon BC2F2 population evaluated in an upland environment , 2001, Theoretical and Applied Genetics.

[6]  Pamela S Soltis,et al.  Genome-scale data, angiosperm relationships, and "ending incongruence": a cautionary tale in phylogenetics. , 2004, Trends in plant science.

[7]  Susceptibility of rice to sheath blight: an assessment of the diversity of rice germplasm according to genetic groups and morphological traits , 2011, Euphytica.

[8]  G. King,et al.  Exploring and exploiting epigenetic variation in crops. , 2010, Genome.

[9]  S. Turner,et al.  Real-Time DNA Sequencing from Single Polymerase Molecules , 2009, Science.

[10]  Norikuni Saka,et al.  Loss of Function of a Proline-Containing Protein Confers Durable Disease Resistance in Rice , 2009, Science.

[11]  Michael J. Thomson,et al.  Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson , 2003, Theoretical and Applied Genetics.

[12]  C. Bustamante,et al.  Genomic Diversity and Introgression in O. sativa Reveal the Impact of Domestication and Breeding on the Rice Genome , 2010, PloS one.

[13]  F. J. Zimmermann,et al.  Construção de uma coleção nuclear de arroz para o Brasil , 2005 .

[14]  D. Zamir.  Improving plant breeding with exotic genetic libraries , 2001, Nature Reviews Genetics.

[15]  Mark H. Wright,et al.  Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa , 2011, Nature communications.

[16]  Lanzhi Li,et al.  Dominance, Overdominance and Epistasis Condition the Heterosis in Two Heterotic Rice Hybrids , 2008, Genetics.

[17]  Y. Ilnytskyy,et al.  Transgenerational Adaptation of Arabidopsis to Stress Requires DNA Methylation and the Function of Dicer-Like Proteins , 2010, PloS one.

[18]  H D Upadhyaya,et al.  Accessing genetic diversity for crop improvement. , 2010, Current opinion in plant biology.

[19]  Jinhua Xiao,et al.  Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa , 2007, Euphytica.

[20]  M. V. D. van der Heijden,et al.  The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. , 2008, Ecology letters.

[21]  F Alex Feltus,et al.  The Association of Multiple Interacting Genes with Specific Phenotypes in Rice Using Gene Coexpression Networks1[C][W][OA] , 2010, Plant Physiology.

[22]  Jun Xiao,et al.  Rice Gene Network Inferred from Expression Profiling of Plants Overexpressing OsWRKY13, a Positive Regulator of Disease Resistance , 2008 .

[23]  C. Wiel,et al.  Distribution of genetic diversity in wild European populations of prickly lettuce (Lactuca serriola): implications for plant genetic resources management , 2010, Plant Genetic Resources.

[24]  R. Fernando,et al.  Linear models for joint association and linkage QTL mapping , 2009, Genetics Selection Evolution.

[25]  Hyuna Yang,et al.  On the subspecific origin of the laboratory mouse , 2007, Nature Genetics.

[26]  Jinhua Xiao,et al.  QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African (O. glaberrima S.) rice. , 2004, Genome.

[27]  Amanda J. Garris,et al.  Genetic Structure and Diversity in Oryza sativa L. , 2005, Genetics.

[28]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[29]  M. Purugganan,et al.  Genomic Variation in Rice: Genesis of Highly Polymorphic Linkage Blocks during Domestication , 2006, PLoS genetics.

[30]  H. Upadhyaya,et al.  Identification of geographical gaps in the pearl millet germplasm conserved at ICRISAT genebank from West and Central Africa , 2009, Plant Genetic Resources.

[31]  P. Marri,et al.  Identification and mapping of yield and yield related QTLs from an Indian accession of Oryza rufipogon , 2005, BMC Genetics.

[32]  M. Metzker.  Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[33]  S. Tanksley,et al.  Seed banks and molecular maps: unlocking genetic potential from the wild. , 1997, Science.

[34]  L. Pollak.  The History and Success of the public–private project on germplasm enhancement of maize (GEM) , 2003 .

[35]  J. Bennetzen,et al.  Dynamic Evolution of Oryza Genomes Is Revealed by Comparative Genomic Analysis of a Genus-Wide Vertical Data Set[W][OA] , 2008, The Plant Cell Online.

[36]  M. Zhang,et al.  Natural Genetic Variation in Selected Populations of Arabidopsis thaliana Is Associated with Ionomic Differences , 2010, PloS one.

[37]  M. Yano,et al.  Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms , 2010, BMC Genomics.

[38]  K. Meyer,et al.  Microbiology of the phyllosphere: a playground for testing ecological concepts , 2011, Oecologia.

[39]  W. Powell,et al.  From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. , 2008, Current opinion in plant biology.

[40]  Z. Chen,et al.  Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. , 2007, Annual review of plant biology.

[41]  C. Bustamante,et al.  Development of genome-wide SNP assays for rice , 2010 .

[42]  F. Allendorf,et al.  Introduction: Population Biology, Evolution, and Control of Invasive Species , 2003 .

[43]  David M. A. Martin,et al.  Genome sequence and analysis of the tuber crop potato , 2011, Nature.

[44]  M. Lorieux,et al.  Chromosome Segment Substitution Lines: A Powerful Tool for the Introgression of Valuable Genes from Oryza Wild Species into Cultivated Rice (O. sativa) , 2010, Rice.

[45]  J. Andrews,et al.  The Ecology and Biogeography of Microorganisms on Plant Surfaces. , 2000, Annual review of phytopathology.

[46]  Y. Sano,et al.  Allelic diversification at the wx locus in landraces of Asian rice , 2008, Theoretical and Applied Genetics.

[47]  Rajeev K. Varshney,et al.  Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties , 2006, Proceedings of the National Academy of Sciences.

[48]  R. Hoekstra,et al.  Analysis of the wild potato germplasm of the series Acaulia with AFLPs: implications for ex situ conservation , 2002, Theoretical and Applied Genetics.

[49]  S. Tanksley,et al.  Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines , 1996, Theoretical and Applied Genetics.

[50]  Lincoln Stein,et al.  The Plant Ontology Database: a community resource for plant structure and developmental stages controlled vocabulary and annotations , 2008, Nucleic Acids Res..

[51]  E. Pauw,et al.  Predictive Association between Biotic Stress Traits and Eco-Geographic Data for Wheat and Barley Landraces , 2011 .

[52]  B. Keller,et al.  Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus , 2009, Proceedings of the National Academy of Sciences.

[53]  A. Jarvis,et al.  Biogeography of wild Arachis: Assessing conservation status and setting future priorities , 2003 .

[54]  A. Jarvis,et al.  A Gap Analysis Methodology for Collecting Crop Genepools: A Case Study with Phaseolus Beans , 2010, PloS one.

[55]  V. Chinnusamy,et al.  Abscisic acid-mediated epigenetic processes in plant development and stress responses. , 2008, Journal of integrative plant biology.

[56]  D. Zamir,et al.  An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. , 1995, Genetics.

[57]  C. Ballaré,et al.  Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. , 2010, Molecular plant-microbe interactions : MPMI.

[58]  Kenneth L. McNally,et al.  Genomewide SNP variation reveals relationships among landraces and modern varieties of rice , 2009, Proceedings of the National Academy of Sciences.

[59]  T. Sang,et al.  Phylogeny of rice genomes with emphasis on origins of allotetraploid species. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Yoichiro Kojima,et al.  Development of mini core collection of Japanese rice landrace , 2008 .

[61]  E. C. J. Groot,et al.  Marker-assisted reduction of redundancy in a genebank collection of cultivated lettuce , 2010, Plant Genetic Resources.

[62]  M. Yano,et al.  Germplasm enhancement by developing advanced plant materials from diverse rice accessions , 2010 .

[63]  R. MacCurdy,et al.  Three-Dimensional Root Phenotyping with a Novel Imaging and Software Platform1[C][W][OA] , 2011, Plant Physiology.

[64]  Aaron J. Lorenz,et al.  Genomic Selection in Plant Breeding , 2011 .

[65]  N. Smith,et al.  Gene Banks and the World's Food , 1987 .

[66]  P. Gupta,et al.  Single nucleotide polymorphisms: A new paradigm for molecular marker technology and DNA polymorphism detection with emphasis on their use in plants , 2001 .

[67]  Qifa Zhang,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

[68]  Massimo Pigliucci,et al.  What Role Does Heritable Epigenetic Variation Play in Phenotypic Evolution? , 2010 .

[69]  R. Hoekstra,et al.  Genetic and economic aspects of marker-assisted reduction of redundancy from a wild potato germplasm collection , 2004, Genetic Resources and Crop Evolution.

[70]  P. Etter,et al.  Rapid SNP Discovery and Genetic Mapping Using Sequenced RAD Markers , 2008, PloS one.

[71]  M. Fitzgerald,et al.  The origin and evolution of fragrance in rice (Oryza sativa L.) , 2009, Proceedings of the National Academy of Sciences.

[72]  Brian D. Ondov,et al.  Efficient mapping of Applied Biosystems SOLiD sequence data to a reference genome for functional genomic applications , 2008, Bioinform..

[73]  Y. Kim,et al.  Fine mapping of a yield-enhancing QTL cluster associated with transgressive variation in an Oryza sativa × O. rufipogon cross , 2008, Theoretical and Applied Genetics.

[74]  F. Jin,et al.  Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon , 2006, Theoretical and Applied Genetics.

[75]  Chenwu Xu,et al.  Developing high throughput genotyped chromosome segment substitution lines based on population whole-genome re-sequencing in rice (Oryza sativa L.) , 2010, BMC Genomics.

[76]  J. Staub,et al.  The Formation of Test Arrays and a Core Collection in Cucumber Using Phenotypic and Molecular Marker Data , 2002 .

[77]  S. Jackson,et al.  The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. , 2005, Genome research.

[78]  C. Nusbaum,et al.  ALLPATHS: de novo assembly of whole-genome shotgun microreads. , 2008, Genome research.

[79]  Zuofeng Zhu,et al.  Construction of introgression lines carrying wild rice (Oryza rufipogon Griff.) segments in cultivated rice (Oryza sativa L.) background and characterization of introgressed segments associated with yield-related traits , 2006, Theoretical and Applied Genetics.

[80]  Jonathan F Wendel,et al.  Genetic and Epigenetic Consequences of Recent Hybridization and Polyploidy in Spartina (poaceae) , 2022 .

[81]  M. Baum,et al.  Sources of resistance in bread wheat to Russian wheat aphid (Diuraphis noxia) in Syria identified using the Focused Identification of Germplasm Strategy (FIGS) , 2011 .

[82]  M. Gore,et al.  Status and Prospects of Association Mapping in Plants , 2008 .

[83]  Tomoko Ito,et al.  Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. , 2010, Molecular Genetics and Genomics.

[84]  M. Smale,et al.  Demand for Genetic Resources and the U.S. National Plant Germplasm System , 2006 .

[85]  B. Vosman,et al.  The distribution of genetic diversity in a Brassica oleracea gene bank collection related to the effects on diversity of regeneration, as measured with AFLPs , 2007, Theoretical and Applied Genetics.

[86]  C. Bustamante,et al.  Global Dissemination of a Single Mutation Conferring White Pericarp in Rice , 2007, PLoS genetics.

[87]  Gloria M. Coruzzi,et al.  The Impact of Outgroup Choice and Missing Data on Major Seed Plant Phylogenetics Using Genome-Wide EST Data , 2009, PloS one.

[88]  F. Carrari,et al.  A candidate gene survey of quantitative trait loci affecting chemical composition in tomato fruit , 2008, Journal of experimental botany.

[89]  J. Glaszmann.  Isozymes and classification of Asian rice varieties , 1987, Theoretical and Applied Genetics.

[90]  A. Rafalski.  Applications of single nucleotide polymorphisms in crop genetics. , 2002, Current opinion in plant biology.

[91]  Xuehui Huang,et al.  High-throughput genotyping by whole-genome resequencing. , 2009, Genome research.

[92]  M. Pigliucci,et al.  Epigenetics for ecologists. , 2007, Ecology letters.

[93]  Keyan Zhao,et al.  Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping , 2011, PLoS genetics.

[94]  M. Yano,et al.  Towards the Understanding of Complex Traits in Rice: Substantially or Superficially? , 2009, DNA research : an international journal for rapid publication of reports on genes and genomes.

[95]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[96]  M. Widrlechner.  Managerial tools for seed regeneration , 1997 .

[97]  S. Jackson,et al.  Orthologous comparisons of the Hd1 region across genera reveal Hd1 gene lability within diploid Oryza species and disruptions to microsynteny in Sorghum. , 2010, Molecular biology and evolution.

[98]  A. McClung,et al.  Development and evaluation of a core subset of the USDA rice germplasm collection , 2007 .

[99]  Ivana V. Yang,et al.  Genetic analysis of complex traits in the emerging Collaborative Cross. , 2011, Genome research.

[100]  Nengjun Yi,et al.  The Collaborative Cross, a community resource for the genetic analysis of complex traits , 2004, Nature Genetics.

[101]  David J Munroe,et al.  Third-generation sequencing fireworks at Marco Island , 2010, Nature Biotechnology.

[102]  N. Sarla,et al.  Oryza glaberrima : A source for the improvement of Oryza sativa , 2005 .

[103]  Jun Xiao,et al.  Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. , 2008, Molecular plant.

[104]  M. Widrlechner,et al.  Analysis of germplasm distribution patterns for collections held at the North Central Regional Plant Introduction Station, Ames, Iowa, USA , 2003, Genetic Resources and Crop Evolution.

[105]  M. Vicente,et al.  Molecular markers for genebank management , 2005 .

[106]  D. Brar,et al.  Alien introgression in rice , 1997, Plant Molecular Biology.

[107]  G. Bending,et al.  Phyllosphere microbiology with special reference to diversity and plant genotype , 2008, Journal of applied microbiology.

[108]  C. Spillane,et al.  Core collections of plant genetic resources. , 2000 .

[109]  M. Sorrells,et al.  Genomic Selection for Crop Improvement , 2009 .

[110]  Jun Wang,et al.  Analysis of 142 genes resolves the rapid diversification of the rice genus , 2008, Genome Biology.

[111]  Ming Chen,et al.  PRIN: a predicted rice interactome network , 2011, BMC Bioinformatics.

[112]  K. Street,et al.  Swimming in the genepool - a rational approach to exploiting large genetic resource collections , 2008 .

[113]  Scott Jackson,et al.  Molecular evidence for a single evolutionary origin of domesticated rice , 2011, Proceedings of the National Academy of Sciences.

[114]  O. H. Frankel,et al.  Genetic perspectives of germplasm conservation , 1984 .

[115]  C. Bustamante,et al.  Selective sweep mapping of genes with large phenotypic effects. , 2005, Genome research.

[116]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.

[117]  Kenneth L. McNally,et al.  Development of a Research Platform for Dissecting Phenotype–Genotype Associations in Rice (Oryza spp.) , 2010, Rice.

[118]  S. Jackson,et al.  Exceptional lability of a genomic complex in rice and its close relatives revealed by interspecific and intraspecific comparison and population analysis , 2011, BMC Genomics.

[119]  M. Kawase,et al.  Development of an RFLP-based Rice Diversity Research Set of Germplasm , 2005 .

[120]  M. McMullen,et al.  Genetic Properties of the Maize Nested Association Mapping Population , 2009, Science.

[121]  M. McMullen,et al.  A unified mixed-model method for association mapping that accounts for multiple levels of relatedness , 2006, Nature Genetics.

[122]  Lauren McIntyre,et al.  Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana , 2003, Nature Biotechnology.

[123]  R. Serraj,et al.  Rice near-isogenic-lines (NILs) contrasting for grain yield under lowland drought stress , 2011 .

[124]  M. T. Jackson,et al.  Genetic erosion over time of rice landrace agrobiodiversity , 2009, Plant Genetic Resources.

[125]  H. Nguyen,et al.  Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, ORYZA RUFIPOGON Griff., into indica rice (Oryza sativa L.) , 2003, Theoretical and Applied Genetics.

[126]  S. Tanksley,et al.  Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. , 1998, Genetics.

[127]  Ernesto Picardi,et al.  Bioinformatics approaches for genomics and post genomics applications of next-generation sequencing , 2010, Briefings Bioinform..

[128]  R. Bernardo.  Molecular Markers and Selection for Complex Traits in Plants: Learning from the Last 20 Years , 2008 .

[129]  Kosuke M. Teshima,et al.  Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice , 2009, Proceedings of the National Academy of Sciences.