Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Lucero, Mary E ^a   Unc, Adrian ^b   Cooke, Peter ^b   Dowd, Scot ^c   Sun, Shulei ^d  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b NEW MEXICO STATE UNIVERSITY   (United States)

^c Research and Testing Laboratory   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASCOMYCETES; ATRIPLEX; ATRIPLEX CANESCENS; ATRIPLEX TORREYI; BACTERIUM IDENTIFICATION; BIOFILM; CONTROLLED STUDY; ENDOPHYTE; FUNGUS IDENTIFICATION; HOST; INTERCELLULAR SPACE; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT CELL; PLANT LEAF; PLANT ROOT; PYROSEQUENCING; SEQUENCE ANALYSIS; BACTERIUM; BAYES THEOREM; BIODIVERSITY; CYTOLOGY; DNA SEQUENCE; FUNGUS; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT SEED; REGENERATION; ULTRASTRUCTURE;

ATRIPLEX; ATRIPLEX CANESCENS; ATRIPLEX TORREYI; BACTERIA (MICROORGANISMS);

SPACER DNA;

ATRIPLEX; BACTERIA; BASE SEQUENCE; BAYES THEOREM; BIODIVERSITY; DNA, INTERGENIC; FUNGI; GERMINATION; METAGENOME; MOLECULAR SEQUENCE DATA; REGENERATION; SEEDS; SEQUENCE ANALYSIS, DNA;

EID: 79952748980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017693     Document Type: Article

References (76)

1. Cibils AF, Swift DM, Hart RH, (2000) Gender-related differences of shrubs in stands of Atriplex canescens with different histories of grazing by cattle. Journal of Arid Environments 46: 383-396.
2. McKeon C, Glenn EP, Waugh WJ, Eastoe C, Jordan F, et al. (2006) Growth and water and nitrate uptake patterns of grazed and ungrazed desert shrubs growing over a nitrate contamination plume. Journal of Arid Environments 64: 1-21.
3. Sawalha MF, Peralta-Videa JR, Parsons JG, Gonzalez JH, Gardea-Torresdey JL, (2008) Removal of cadmium from contaminated waters using saltbush (Atriplex canescens) biomass: Identification of Cd binding sites. International Journal of Environment and Pollution 34: 28-42.
4. Sanderson SC, McArthur ED, (2004) Fourwing saltbush (Atriplex canescens) seed transfer zones. USDA Forest Service- General Technical Report RMRS-GTR pp. 1-13.
5. Stutz HC, (1978) Explosive evolution of perennial Atriplex in western America.In: Harper KT, Reveal JL, editors. Great Basin Naturalist Memoirs 276 North America Western North American Naturalist Publications.
6. Glenn E, Tanner R, Miyamoto S, Fitzsimmons K, Boyer J, (1998) Water use, productivity and forage quality of the halophyte Atriplex nummularia grown on saline waste water in a desert environment. Journal of Arid Environments 38: 45-62.
7. Sawalha MF, Peralta-Videa JR, Romero-Gonzalez J, Duarte-Gardea M, Gardea-Torresdey JL, (2007) Thermodynamic and isotherm studies of the biosorption of Cu(II), Pb(II), and Zn(II) by leaves of saltbush (Atriplex canescens). Journal of Chemical Thermodynamics 39: 488-492.
8. McArthur ED, Freeman DC, Luckinbill LS, Sanderson SC, Noller GL, (1992) Are Trioecy and Sexual Lability in Atriplex canescens Genetically Based?: Evidence from Clonal Studies. Evolution 46: 1708-1721.
9. Rodriguez R, Redman R, (2008) More than 400 million years of evolution and some plants still can't make it on their own: Plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109-1114.
10. Miller RM, Moorman TB, Schmidt SK, (1983) Interspecific plant association effects on vesicular-arbuscular mycorrhiza occurrence in Atriplex confertifolia. New Phytologist 95: 241-246.
11. Asghari HR, Marschner P, Smith SE, Smith FA, (2005) Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant and Soil 273: 245-256.
12. Barrow JR, Aaltonen RE, (2001) Evaluation of the internal colonization of Atriplex canescens (pursh) nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11: 199-205.
13. Barrow JR, Osuna P, (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. Journal of Arid Environments 51: 449-459.
14. Mandyam K, Jumpponen A, (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in Mycology 53: 173-189.
15. Barrow JR, Havstad KM, Hubstenberger J, McCaslin BD, (1997) Seed-borne fungal endophytes on fourwing saltbush, Atriplex canescens. Arid Soil Research and Rehabilitation 11: 307-314.
16. Barrow JR, Osuna-Avila P, Reyes-Vera I, (2004) Fungal endophytes intrinsically associated with micropropagated plants regenerated from native Bouteloua eriopoda Torr. and Atriplex canescens (Pursh) Nutt. In Vitro Cellular and Developmental Biology- Plant 40: 608-612.
17. Clay K, (1996) Interactions among Fungal Endophytes, Grasses and Herbivores. Researches on Population Ecology 38: 191-201.
18. Rudgers JA, Clay K, (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biology Reviews 21: 107-124.
19. Rudgers JA, Koslow JM, Clay K, (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecology Letters 7: 42-51.
20. Zhuang J, Marchant MA, Schardl CL, Butler CM, (2005) Economic analysis of replacing endophyte-infected with endophyte-free tall fescue pastures. Agronomy Journal 97: 711-716.
21. Bacon CW, Richardson MD, White JF Jr, (1997) Modification and uses of endophyte-enhanced turfgrasses: A role for molecular technology. Crop Science 37: 1415-1425.
22. Braun K, Romero J, Liddell C, Creamer R, (2003) Production of swainsonine by fungal endophytes of locoweed. Mycological Research 107: 980-988.
23. Petroski RJ, Powell RG, Clay K, (1992) Alkaloids of Stipa robusta (sleepygrass) infected with an Acremonium endophyte. Natural toxins 1: 84-88.
24. Ralphs MH, Creamer R, Baucom D, Gardner DR, Welsh SL, et al. (2007) Relationship Between the Endophyte Embellisia spp. and the Toxic Alkaloid Swainsonine in Major Locoweed Species (Astragalus and Oxytropis). Journal of Chemical Ecology pp. 1-9.
25. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS, (2009) Fungal endophytes: Diversity and functional roles: Tansley review. New Phytologist 182: 314-330.
26. Lucero ME, Barrow JR, Osuna P, Reyes I, (2006) Plant-fungal interactions in arid and semi-arid ecosystems: Large-scale impacts from microscale processes. Journal of Arid Environments 65: 276-284.
27. Lucero ME, Barrow JR, Osuna P, Reyes I, Duke SE, (2008) Enhancing native grass productivity by cocultivating with endophyte-laden calli. Rangeland Ecology and Management 61: 124-130.
28. Wagner WL, Earl A, (1978) A Manual of the Saltbushes (Atriplex spp.) in New Mexico. Rocky Mountain Forest and Range Experiment Station.
29. Gibbens RP, McNeely RP, Havstad KM, Beck RF, Nolen B, (2005) Vegetation changes in the Jornada Basin from 1858 to 1998. Journal of Arid Environments 61: 651-668.
30. Reyes-Vera I, Lucero M, Barrow J, (2010) An improved protocol for micropropagation of saltbush (Atriplex) species. Native Plants Journal 11: 53-56.
31. Murashige T, Skoog F, (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiology 15: 473-497.
32. Callaway TR, Dowd SE, Wolcott RD, Sun Y, McReynolds JL, et al. (2009) Evaluation of the bacterial diversity in cecal contents of laying hens fed various molting diets by using bacterial tag-encoded FLX amplicon pyrosequencing. Poultry Science 88: 298-302.
33. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, et al. (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology 8.
34. Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA, (2008) Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: Bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathogens and Disease 5: 459-472.
35. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, et al. (2008) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS ONE 3.
36. Acosta-Martinez V, Dowd SE, Sun Y, Allen V, (2009) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biology and Biochemistry 41: 2762-2770.
37. Li W, (2009) Analysis and comparison of very large metagenomes with fast clustering and functional annotation. BMC Bioinformatics 10.
38. Li W, Godzik A, (2006) Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
39. Seshadri R, Kravitz S, Smarr L, Gilna P, Frazier M, (2007) CAMERA: A Community Resource for Metagenomics. PLoS Biology 5.
40. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261-5267.
41. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37: D141-D145.
42. Martin KJ, Rygiewicz PT, (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology 5.
43. Spatafora JW, (2005) Assembling the fungal tree of life (AFTOL). Mycological Research 109: 755-756.
44. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
45. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
46. Kwok E, Hanson M, (2004) Plastids and stromules interact with the nucleus and cell membrane in vascular plants. Plant Cell Reports 23: 188-195.
47. Pighin J, Zheng H, Balakshin L, Goodman I, Western T, et al. (2004) Plant cuticular lipid export requires an ABC transporter. Science 306: 702.
48. Fett WF, Cooke PH, (2005) A survey of native microbial aggregates on alfalfa, clover and mung bean sprout cotyledons for thickness as determined by confocal scanning laser microscopy. Food Microbiology 22: 253-259.
49. Handelsman J, Tiedje J, Alvarez-Cohen L, Ashburner M, Cann I, et al. (2007) The new science of metagenomics: revealing the secrets of our microbial planet. Washington, DC The National Academies Press.
50. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity for basidiomycetes- application to the identification of mycorrhizae and rusts. Molecular Ecology Notes 2: 113-118.
51. Göbel UB, (1995) Phylogenetic amplification for the detection of uncultured bacteria and the analysis of complex microbiota. Journal of Microbiological Methods 23: 117-128.
52. White TJ, Bruns T, Lee S, Taylor JW, (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications San Diego Academic Press pp. 315-322.
53. Lucero M, Barrow JR, Osuna P, Reyes I, (2008) A cryptic microbial community persists within micropropagated Bouteloua eriopoda (Torr.) Torr. cultures. Plant Science 174: 570-575.
54. Sipos R, Székely A, Révész S, Márialigeti K, (2010) Addressing PCR biases in environmental microbiology studies. Methods in molecular biology 599: 37-58.
55. Karimi SH, Ungar IA, (1989) Development of Epidermal Salt Hairs in Atriplex triangularis Willd. in Response to Salinity, Light Intensity, and Aeration. Botanical Gazette 150: 68-71.
56. Kowalchuk GA, Yergean E, Leveau JHJ, Sessitch A, Bailey M, (2010) Plant associated microbial communities. In: Liu WT, Jansson JK, editors. Environmental Molecular Biology Norfolk, UK Caister Academic Press pp. 131-148.
57. Morris CE, Monier JM, (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annual Review of Phytopathology 41: 429-453.
58. Eberl L, von Bodman SB, Fuqua C, (2007) Biofilms on plant surfaces. In: Kjelleberg S, Givskov M, editors. The Biofilm Mode of Life Mechanisms and Adaptations Norfolk, UK Horizon Bioscience pp. 215-233.
59. Davey M, O'Toole G, (2000) Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews 64: 847-867.
60. Rosenblueth M, Martínez-Romero E, (2006) Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions 19: 827-837.
61. Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM, (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Communitative and Integrative Biology 1: 69-93.
62. Mano H, Morisaki H, (2008) Endophytic bacteria in the rice plant. Microbes and Environments 23: 109-117.
63. Abreu-Tarazi MF, Navarrete AA, Andreote FD, Almeida CV, Tsai SM, et al. (2009) Endophytic bacteria in long-term in vitro cultivated "axenic" pineapple microplants revealed by PCR-DGGE. World Journal of Microbiology and Biotechnology pp. 1-6.
64. Müller P, Döring M, (2009) Isothermal DNA amplification facilitates the identification of a broad spectrum of bacteria, fungi and protozoa in Eleutherococcus sp. plant tissue cultures. Plant Cell, Tissue and Organ Culture 98: 35-45.
65. Thomas P, Kumari S, Swarna GK, Gowda TKS, (2007) Papaya shoot tip associated endophytic bacteria isolated from in vitro cultures and host-endophyte interaction in vitro and in vivo. Canadian Journal of Microbiology 53: 380-390.
66. Vieira de Almeida C, Andreote FD, Yara R, Tanaka FAO, Azevedo JL, et al. (2009) Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World Journal of Microbiology and Biotechnology 25: 1757-1764.
67. Wink M, (2008) Plant secondary metabolism: Diversity, function and its evolution. Natural Product Communications 3: 1205-1216.
68. Berg G, (2009) Plant-microbe interactions promoting plant growth and health: Perspectives for controlled use of microorganisms in agriculture. Applied Microbiology and Biotechnology 84: 11-18.
69. Piotrowski JS, Rillig MC, (2008) Succession of Arbuscular Mycorrhizal Fungi: Patterns, Causes, and Considerations for Organic Agriculture. Advances in Agronomy pp. 111-130.
70. Gallery RE, Dalling JW, Arnold AE, (2007) Diversity, host affinity, and distribution of seed-infecting fungi: A case study with Cecropia. Ecology 88: 582-588.
71. Kluger CG, Dalling JW, Gallery RE, Sanchez E, Weeks-Galindo C, et al. (2008) Host generalists dominate fungal communities associated with seeds of four neotropical pioneer species. Journal of Tropical Ecology 24: 351-354.
72. Saikkonen K, WÃ{currency sign}li P, Helander M, Faeth SH, (2004) Evolution of endophyte-plant symbioses. Trends in Plant Science 9: 275-280.
73. U'Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, et al. (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples. Mycological Research 113: 432-449.
74. Afkhami ME, Rudgers JA, (2008) Symbiosis lost: Imperfect vertical transmission of fungal endophytes in grasses. American Naturalist 172: 405-416.
75. Ishak HD, Plowes R, Sen R, Kellner K, Meyer E, et al. (2011) Bacterial Diversity in Solenopsis invicta and Solenopsis geminata Ant Colonies Characterized by 16S amplicon 454 Pyrosequencing. Microbial Ecology pp. 1-11.
76. Larena I, Salazar O, González V, Julián MC, Rubio V, (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. Journal of Biotechnology 75: 187-194.