Research Articles |
|
|
|
|
Diversity of endophytes across the soil-plant continuum for Atriplex spp. in arid environments |
Mohammad E TAHTAMOUNI1, Sa’eb KHRESAT2, Mary LUCERO1, Jesus SIGALA1,3, Adrian UNC1,4,5* |
1 New Mexico State University, Department of Plant & Environmental Sciences, Las Cruces NM 88003, USA;
2 Jordan University of Science and Technology, Department of Natural Resources and Environment, Irbid 22110, Jordan;
3 Seco Spice, Chamberino NM 88027, USA;
4 Boreal Ecosystems Research Initiative, Memorial University of Newfoundland, Corner Brook A2H 5G4, Canada;
5 University of Leeds, School of Geography, Leeds LS2 9JT, UK |
|
|
Abstract Endophytes are hypothesized to be transferred across the soil-plant continuum, suggesting both the transfers of endophytes from environment to plant and from plant to soil. To verify this hypothesis and to assess the role of locality, we evaluated the similarity of microbial communities commonly found both in soils and endophytic communities in three arid regions, i.e. the Jornada LTER (Long Term Ecological Research) site in New Mexico, USA, and the research station of Jordan University of Science and Technology (JUST) and Khanasri research station in Badia region of Jordan. Rhizosphere and non-rhizosphere soils, leaves and seeds of Atriplex spp. were sampled. Diversity and distribution of bacteria and fungi across the soil-plant continuums were assessed by tag-encoded FLX amplicon pyrosequencing and sequence alignment. Of the total bacterial OTUs (operational taxonomic units), 0.17% in Khanasri research station, 0.16% in research station of JUST, and 0.42% in Jornada LTER site were commonly found across all the plant and soil compartments. The same was true for fungi in two regions, i.e. 1.56% in research station of JUST and 0.86% in Jornada LTER site. However, in Khanasri research station, 12.08% of total fungi OTUs were found in at least one soil compartment and one plant compartment. Putative Arthrobacter, Sporosarcina, Cladosporium and members of Proteobacteria and Actinobacteria were found across all the soil-plant continuums. Ascomycota, mainly including Didymellaceae, Pleosporaceae and Davidiellaceae were present across all the soil-plant continuums. Microbial communities in two regions of Jordan were similar to each other, but both of them were different from the Jornada LTER site of USA. SIMPER (similarity percentage) analysis of bacterial and fungal taxa for both soil and endophyte communities revealed that dissimilarities of two bacterial genera (Arthrobacter and Sporosarcina) and two fungal genera (Cladosporium and Alternaria) are very high, so they play key roles in the soil-plant continuums. A weighed Pearson correlation analysis for the specific bacterial OTUs in the soil-plant continuums only showed high similarity between the two regions of Jordan. However, fungal groups showed higher similarities among all regions. This research supports the hypothesis of continuity of certain bacterial and fungal communities across the soil-plant continuums, and also explores the influences of plant species and geographic specificity on diversity and distribution of bacteria and fungi.
|
Received: 25 April 2015
Published: 01 April 2016
|
Corresponding Authors:
|
|
|
Al-Bakri J T, Ajlouni M, Abu-Zanat M. 2008. Incorporating land use mapping and participation in Jordan: An approach to sustainable management of two mountainous areas. Mountain Research and Development, 28(1): 49–57. Alzweiri M, Al Sarhan A, Mansi K, et al. 2011. Ethnopharmacological survey of medicinal herbs in Jordan, the Northern Badia region. Journal of Ethnopharmacology, 137(1): 27–35. Assmus B, Hutzler P, Kirchhof G, et al. 1995. In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Applied and Environmental Microbiology, 61(3): 1013–1019.Bais H P, Weir T L, Perry L G, et al. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57: 233–266. Barrow J R, Havstad K M, Hubstenberger J, et al. 1997. Seed-borne fungal endophytes on fourwing saltbush, Atriplex canescens. Arid Soil Research Rehabilitation, 11(4): 307–314. Barrow J R, Osuna P. 2002. Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. Journal of Arid Environments, 51(3): 449–459.Barrow J R, 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 & Developmental Biology-Plant, 40(6): 608–612. Barrow J, Lucero M, Reyes-Vera I, et al. 2008. Do symbiotic microbes have a role in regulating plant performance and response to stress? Communicative & Integrative Biology, 1(1): 69–93.Basilio A, González I, Vicente M F, et al. 2003. Patterns of antimicrobial activities from soil actinomycetes isolated under different conditions of pH and salinity. Journal of Applied Microbiology, 95(4): 814–823.Bulgarelli D, Schlaeppi K, Spaepen S, et al. 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology, 64: 807–838.Burdman S, Jurkevitch E, Schwartsburd B, et al. 1999. Involvement of outer-membrane proteins in the aggregation of Azospirillum brasilense. Microbiology, 145(5): 1145–1152. Chi F, Shen S H, Cheng H P, et al. 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Applied Environmental Microbiology, 71(11): 7271–7278. Colwell R K. 2013. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples (version 9.1.0). User’s Guide and Application. http://purl.oclc.org/estimates.Compant S, Mitter B, Colli-Mull J, et al. 2011. Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microbial Ecology, 62(1): 188–197.Dalling J W, Davis A S, Schutte B J, et al. 2011. Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology, 99(1): 89–95. Doty S L. 2008. Enhancing phytoremediation through the use of transgenics and endophytes. New Phytologist, 179(2): 318–333.Fahlgren C, Hagstrom Å, Nilsson D, et al. 2010. Annual variations in the diversity, viability, and origin of airborne bacteria. Applied and Environmental Microbiology, 76(9): 3015–3025.Flynn T M, Sanford R A, Ryu H, et al. 2013. Functional microbial diversity explains groundwater chemistry in a pristine aquifer. BMC Microbiology, 13(1): 146.Gallery R E, Dalling J W, Arnold A E. 2007. Diversity, host affinity, and distribution of seed-infecting fungi: A case study with Cecropia. Ecology, 88(3): 582–588. Gardner T, Acosta-Martinez V, Senwo Z, et al. 2011. Soil rhizosphere microbial communities and enzyme activities under organic farming in Alabama. Diversity, 3(3): 308–328. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5): 696–704.Hammer Ø, Harper D A T, Ryan P D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 1–9.Hardoim P R, Van Overbeek L S, Van Elsas J D. 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology, 16(10): 463–471.Hinrichs K U, Summons R E, Orphan V, et al. 2000. Molecular and isotopic analysis of anaerobic methane-oxidizing communities in marine sediments. Organic Geochemistry, 31(12): 1685–1701.Huson D H, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2): 254–267.Ishak H D, Plowes R, Sen R, et al. 2011. Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 Pyrosequencing. Microbial Ecology, 61(4): 821–831.Johnston-Monje D, Raizada M N. 2012. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography, and ecology. PLoS ONE, 6(6): e20396, doi:10.1371/journal.pone.0020396.Kaplan D, Maymon M, Agapakis C M, et al. 2013. A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae) using cultivation-dependent and cultivation-independent methods. American Journal of Botany, 100(9): 1713–1725.Khair M, El-Shatnawi J, Mohawesh Y M. 2000. Seasonal chemical composition of saltbush in semiarid grasslands of Jordan. Journal of Range Management, 53(2): 211–214.Kumar D, Hyde K D. 2004. Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Diversity, 17: 69–90.Larkin M A, Blackshields G, Brown N P, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21): 2947–2948.Leuchtmann A. 1993. Systematics, distribution, and host specificity of grass endophytes. Journal of Natural Toxins, 1(3): 150–162. Lucero M E, Barrow J R, Osuna P, et al. 2006. Plant-fungal interactions in arid and semiarid ecosystems: large scale impacts from microscale processes. Journal of Arid Environments, 65(2): 276–284.Lucero M E, Barrow J R, Osuna P, et al. 2008. Enhancing native grass productivity by co-cultivating with endophyte-laden calli. Rangeland Ecology and Management, 61(1): 124–130. Lucero M E, Unc A, Cooke P, et al. 2011. Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS ONE, 6(3): e17693, doi: 10.1371/journal.pone.0017693. Lynch J M, Whipps J M. 1991. Substrate flow in the rhizosphere. In: Keister D L, Cregan P B. The Rhizosphere and Plant Growth. Netherlands: Springer, 14: 15–24. Martínez-Falcón A P, Durbán A, Latorre A, et al. 2011. Bacteria associated with Copestylum (Diptera, Syrphidae) larvae and their cactus host Isolatocereus dumortieri. PLoS ONE, 6(11): e27443, doi: 10.1371/journal.pone.0027443.McCully M E. 2001. Niches for bacterial endophytes in crop plants: a plant biologist’s view. Australian Journal of Plant Physiology, 28(9): 983–990.Miranda L N, Hutchison K, Grossman A R, et al. 2013. Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS ONE, 8(3): e58269, doi: 10.1371/journal.pone.0058269.Niu B F, Fu L M, Sun S L, et al. 2010. Artificial and natural duplicates in pyrosequencing reads of metagenomic data. Bioinformatics, 11: 187.Ogle D, St. John L, Tilley D. 2012. Plant guide for fourwing saltbush Atriplex canescens (Pursh) Nutt. In: USDA-Natural Resources Conservation Service, Aberdeen, ID Plant Materials Center. 83210–0296.Oliveros J, Venny C. 2007. An interactive tool for comparing lists with Venn Diagrams. [2015-04-15]. http://bioinfogp.cnb.csic.es/tools/venny/index.html. Peters D P C, Herrick J E, Monger H C, et al. 2010. Soil-vegetation-climate interactions in arid landscapes: effects of the North American monsoon on grass recruitment. Journal of Arid Environments, 74(5): 618–623.Plummer M. 1984. Considerations in selecting chenopod species for range seedings. In: Tiedemann A R, McArthur E D, Stutz H C, et al. Proceedings Symposium on the Biology of Atriplex and Related Chenopods. U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station, 183–186.Saikkonen K, Wäli P, Helander M, et al. 2004. Evolution of endophyte plant symbioses. Trends in Plant Sciences, 9(6): 275–280. Schardl C L, Leuchtmann A, Spiering M J. 2004. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Physiology, 55: 315–340. Shakhatreh Y, Kafawin O, Ceccarelli S, et al. 2001. Selection of barley lines for drought tolerance in low-rainfall areas. Journal of Agronomy and Crop Science, 186(2): 119–127. Sun S L, Chen J, Li W Z, et al. 2010. Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Research, 39(suppl 1): D546–D551. Walker D J, Lutts S, Sánchez-Garcíac M, et al. 2014. Atriplex halimus L.: Its biology and uses. Journal of Arid Environments, 100–101: 111–121.Wang Q, Garrity G M, Tiedje J M, et al. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267. Welsh S L, Atwood N D, Goodrich S, et al. 2003. A Utah Flora (3rd ed.). Provo, UT: Brigham Young University, 1–912.Whitman W B, Coleman D C, Wiebe W J, 1998. Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences of the United States of America, 95(12): 6578–6583.Wilson D. 1995. Endophyte: the evolution of a term, and clarification of its use and definition. Oikos, 73(2): 274–276. |
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|