The contribution of foliar endophytes to quantitative resistance to Melampsora rust.

Foliar endophytes of Populus do not induce the hypersensitive response associated with major genes for resistance to Melampsora leaf rust. But they could contribute to the quantitative resistance that represents a second line of defense. Quantitative resistance is thought to be determined by suites of minor genes in both host and pathogen that are influenced by the abiotic environment. Here, we determined the relative importance to quantitative resistance of foliar endophytes, one element of the biotic environment. Leaves of six host genotypes differing in genetic resistance to Melampsora × columbiana were inoculated first with one of four foliar endophytes (Stachybotrys sp., Trichoderma atroviride, Ulocladium atrum or Truncatella angustata), and then with Melampsora. These endophytes greatly reduced rust severity within inoculated leaves (i.e. local effects), but they had no systemic effect on rust of leaves not inoculated with endophytes. Differences among endophytes and their controls explained 54% of the total variation in quantitative resistance (i.e. rust severity); the six host/pathogen genotypes explained just 5%. In terms of magnitude of effect on rust severity, Stachybotrys, Trichoderma, Ulocladium and Truncatella were ranked in this order on all host/pathogen genotypes. Endophytes may contribute significantly to quantitative resistance to Melampsora in leaves of Populus.

[1]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[2]  J. Stone Initiation and development of latent infections by Rhabdocline parkeri on Douglas-fir , 1987 .

[3]  G. Newcombe,et al.  Abundant Pathogenic Variation in the New Hybrid Rust Melampsora xcolumbiana on Hybrid Poplar. , 2001, Phytopathology.

[4]  G. Newcombe,et al.  A community of unknown, endophytic fungi in western white pine. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Bastien,et al.  Presence of defeated qualitative resistance genes frequently has major impact on quantitative resistance to Melampsora larici-populina leaf rust in P. × interamericana hybrid poplars , 2007, Tree Genetics & Genomes.

[6]  G. Newcombe The specificity of fungal pathogens of Populus , 1996 .

[7]  A. Arnold,et al.  Fungal endophytes: diversity and functional roles. , 2009, The New phytologist.

[8]  D. Tilman,et al.  Fungal endophytes limit pathogen damage in a tropical tree , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. Wedin,et al.  Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance , 2010, Fungal Diversity.

[10]  D. S. St. Clair,et al.  Quantitative disease resistance and quantitative resistance Loci in breeding. , 2010, Annual review of phytopathology.

[11]  R. H. Biffen Mendel's Laws of Inheritance and Wheat Breeding , 1905, The Journal of Agricultural Science.

[12]  A. Arnold,et al.  Endophytic fungi as biocontrol agents of Theobroma cacao pathogens , 2008 .

[13]  G. Chastagner,et al.  A major gene for resistance to Melampsora medusae f. sp. deltoidae in a hybrid poplar pedigree , 1996 .

[14]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[15]  A. Arnold,et al.  Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers , 2007 .

[16]  C. Pieterse,et al.  Plant immune responses triggered by beneficial microbes. , 2008, Current opinion in plant biology.

[17]  G. May,et al.  Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. , 2009, FEMS microbiology letters.

[18]  T. Hinckley,et al.  Biology of populus and its implications for management and conservation , 1996 .

[19]  Thomas J. White,et al.  PCR protocols: a guide to methods and applications. , 1990 .

[20]  D. Dickmann,et al.  Poplar culture in North America , 2001 .

[21]  C. Pieterse,et al.  Systemic resistance induced by rhizosphere bacteria. , 1998, Annual review of phytopathology.

[22]  M. Villar,et al.  A Single Gene Cluster Controls Incompatibility and Partial Resistance to Various Melampsora larici-populina Races in Hybrid Poplars. , 1998, Phytopathology.

[23]  O. Santamaría,et al.  Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain , 2005 .

[24]  H. Nakayashiki,et al.  Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. , 2005, Molecular plant-microbe interactions : MPMI.

[25]  L. Sequeira Cross protection and induced resistance: their potential for plant disease control , 1984 .

[26]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[27]  S. E. Thomas,et al.  Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species , 2006, Planta.

[28]  W. Q. Loegering Current concepts in interorganismal genetics , 1978 .

[29]  K. S. Chester The Problem of Acquired Physiological Immunity in Plants , 1933, The Quarterly Review of Biology.

[30]  J. Bever,et al.  Genotype, environment, and genotype by environment interactions determine quantitative resistance to leaf rust (Coleosporium asterum) in Euthamia graminifolia (Asteraceae). , 2004, The New phytologist.

[31]  Van der Plank Disease resistance in plants , 1969 .

[32]  G. Newcombe Association of Mmd1, a Major Gene for Resistance to Melampsora medusae f. sp. deltoidae, with Quantitative Traits in Poplar Rust. , 1998, Phytopathology.

[33]  C. Bastien,et al.  Partial Resistance to Melampsora larici-populina Leaf Rust in Hybrid Poplars: Genetic Variability in Inoculated Excised Leaf Disk Bioassay and Relationship with Complete Resistance. , 2003, Phytopathology.

[34]  G. Newcombe,et al.  Endophyte-mediated resistance against white pine blister rust in Pinus monticola , 2008 .