Skip to main content

Advertisement

SpringerLink
Log in

Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Since root endophytes may ameliorate drought stress, understanding which plants associate with endophytes is important, especially in arid ecosystems. Here, the root endophytes were characterized of 42 plants from an arid region of Argentina. Colonization by arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSEs) was related to plant functional type (PFT), family, and phylogenetic relatedness. Overall, three main findings were observed. Firstly, only moderate levels of endophyte associations were found across all taxa (e.g., most Poaceae were not colonized by endophytes despite numerous accounts of colonization by AMF and DSEs). We determined 69 % of plant taxa associated with some form of root endophyte but levels were lower than other regional studies. Secondly, comparisons by PFT and phylogeny were often qualitatively similar (e.g., succulents and Portulacineae consistently lacked AMF; variation occurred among terrestrial vs. epiphytic bromeliads) and often differed from comparisons based on plant family. Thirdly, comparisons by plant family often failed to account for important variation either within families (e.g., Bromeliaceae and Poaceae) or trait conservatism among related families (i.e., Rosidae consistently lacked DSEs and Portulacineae lacked AMF). This study indicates the value of comparing numerous taxa based on PFTs and phylogenetic similarity. Overall, the results suggest an uncertain benefit of endophytes in extremely arid environments where plant traits like succulence may obviate the need to establish associations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247

    Article  CAS  PubMed  Google Scholar 

  • Barrow JR, Osuna P (2002) Phosphorous solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J Arid Environ 51:449–459

    Article  Google Scholar 

  • Bobich EG, North GB (2009) Structural implications of succulence: architecture, anatomy, and mechanics of photosynthetic stem, pachycauls, and leaf succulents. In: De la Barrera E, Smith WK (eds) Perspective in biophysical plant ecophysiology: a tribute to Park S. Nobel. UNAM, México, pp 3–37

    Google Scholar 

  • Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    Article  CAS  Google Scholar 

  • Cabrera AL (1976) Territorios fitogeográficos de la República Argentina. Enciclopedia Argentina de Agricultura y Jardinería, 2nd ed, II (1). ACME, Argentina

  • Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH (2009) Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS One 4:e5695

    Article  PubMed Central  PubMed  Google Scholar 

  • Capitanelli R (1989) Geografía de San Luis. Gobierno de la Prov. de San Luis. Ministerio de Cultura y Educación, pp 205–216

  • Chaudhry MS, Nasim FH, Khan AG (2006) Mycorrhizas in the perennial grasses of Cholistan Desert, Pakistan. Int J Bot 2:210–218

    Article  Google Scholar 

  • Crayn DM, Winter K, Smith JC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. PNAS 101:3703–3708

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Del Vitto LA, Petenatti EM, Petenatti ME (2001) Catálogo preliminar de la Flora Vascular, Parque Nacional “Sierra de las Quijadas” San Luis, Argentina. Serie Técnica del Herbario UNSL 8:1–13

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 35:1792–1797

    Article  Google Scholar 

  • Fracchia S, Aranda A, Gopar A, Silvani V, Fernández L, Godeas A (2009) Mycorrhizal status of plant species in the Chaco Serrano woodland from central Argentina. Mycorrhiza 19:205–214

    Article  PubMed  Google Scholar 

  • Fritz SA, Purvis A (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24:1042–1051

    Article  PubMed  Google Scholar 

  • Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162

    Article  Google Scholar 

  • Hetrick BAD, Kitt DG, Wilson GWT (1988) Mycorrhizal dependence and growth habit of warm-season and cool-season tallgrass prairie plants. Can J Bot 66:1376–1380

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Todd TC (1990) Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, phosphorus fertilization, and soil microorganisms. Can J Bot 68:461–467

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Leslie JF (1991) Root architecture to warm- and cool-season grasses: relationship to mycorrhizal dependence. Can J Bot 69:112–118

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Todd TC (1992) Relationships of mycorrhizal symbiosis, rooting strategy, and phenology among tallgrass prairie forbs. Can J Bot 70:1521–1528

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310

    Article  Google Scholar 

  • Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious—dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS ONE 7(1–8):e32570

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kohn LM, Stasovski E (1990) The mycorrhizal status of plants at Alexandra Fiord, Ellesmere Island, Canada, a High Arctic site. Mycologia 82:23–35

    Article  Google Scholar 

  • Kovács GM, Szigetvári C (2002) Mycorrhizae and other root-associated fungal structures of the plants of a sandy grassland on the Great Hungarian Plain. Phyton 42:211–223

    Google Scholar 

  • Kress WJ, Erickson DL, Jones FA, Swenson NG, Perez R, Sanjur O (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. PNAS 106:18621–18626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lingfei L, Anna Y, Zhiwei A (2005) Seasonality of arbuscular mycorrhizal simbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol Ecol 54:367–373

    Article  PubMed  Google Scholar 

  • Lugo MA, González Maza ME, Cabello MN (2003) Arbuscular mycorrhizal fungi in a mountain grassland II: seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95:407–415

    Article  PubMed  Google Scholar 

  • Lugo MA, Anton AN, Cabello MN (2005) Arbuscular mycorrhizas in the Larrea divaricata shrubland at arid “Chaco”, Central Argentina. J Agric Tech 1:163–178

    Google Scholar 

  • Lugo MA, Menoyo E, Negritto MA, Anton AN (2007) Micorrizas arbusculares versus “septados oscuros” en pastos puneños. Bol Soc Argent Bot 42(Supl. 2007):210

    Google Scholar 

  • Lugo MA, Negritto MA, Jofré M, Anton A, Galetto L (2012) Colonization of native Andean grasses by arbuscular mycorrhizal fungi in Puna: a matter of altitude, host photosynthetic pathway and host life cycles. FEMS Microbiol Ecol 81:455–466

    Article  CAS  PubMed  Google Scholar 

  • Mandyam K, Fox C, Jumpponen A (2012) Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie. Mycorrhiza 22:109–119

    Article  PubMed  Google Scholar 

  • Marins J, Fraccaro DE, Carrenho R, Thomaz SM (2009) Occurrence and coexistence of arbuscular mycorrhizal fungi and dark septate fungi in aquatic macrophytes in a tropical river–floodplain system. Aquat Bot 91:13–19

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild DL, Swam JA (1990) A new methods which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M (2005) A brief history of seed size. Science 307:576–580

    Article  CAS  PubMed  Google Scholar 

  • Ness JH, Rollinson EJ, Whitney KD (2011) Phylogenetic distance predicts susceptibility to attack by natural enemies. Oikos 120:1327–1334

    Article  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793

    Article  CAS  PubMed  Google Scholar 

  • Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20

    Article  Google Scholar 

  • Nylander JA (2004) MrModeltest v2. [2.13]. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2013) Caper: Comparative Analyses of Phylogenetics and Evolution in R. Version 0.5.2. http://CRAN.R-project.org/package=caper

  • Pérez M, Urcelay C (2009) Differential growth response to arbuscular mycorrhizal fungi and plant density in two wild plants belonging to contrasting functional types. Mycorrhiza 19:517–523

    Article  PubMed  Google Scholar 

  • Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl Environ Microbiol 74:2805–2813

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B Biol Sci 276:4237–4245

    Article  Google Scholar 

  • Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytol 88:341–352

    Article  Google Scholar 

  • Reinhart KO, Wilson GWT, Rinella MJ (2012) Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecol Lett 689–695

  • Rivarola D (1997) El Parque Nacional Sierra de las Quijadas y sus recursos naturales. Printers Impresores, Argentina

    Google Scholar 

  • Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170:357–368

    Article  PubMed  Google Scholar 

  • Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW (2008) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and Rocky Mountains. Arct Antarct Alp Res 40:576–583

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Sraj-Krzic N, Pongrac P, Klemenc M, Kladnik A, Regvar M, Gaberscik A (2006) Mycorrhizal colonization in plants from intermitent aquatic habitats. Aquat Bot 85:331–336

    Article  Google Scholar 

  • Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhyzal plants. CRC Press, Boca Raton, Florida, pp 5–25

    Google Scholar 

  • Urcelay C, Battistella R (2007) Colonización micorrícica en distintos tipos funcionales de plantas herbáceas del centro de Argentina. Ecología Austral 17:179–188

    Google Scholar 

  • Urcelay C, Acho J, Joffre R (2011) Fungal root symbionts and their relationship with fine root proportion in native plants from the Bolivian Andean highlands above 3,700 m elevation. Mycorrhiza 21:323–330

    Article  PubMed  Google Scholar 

  • Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  CAS  PubMed  Google Scholar 

  • Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183

    Article  Google Scholar 

  • Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100

    Article  CAS  PubMed  Google Scholar 

  • Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall, Inc., Upper Saddle River, New Jersey

    Google Scholar 

Download references

Acknowledgments

We are grateful to Brian Anacker for comments on the manuscript. This work was supported by grants from PROICO 2-O203, and PICT 0781-2008. C.U. wish to acknowledge Secyt, Mincyt (Córdoba), and the assistance of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the Universidad Nacional de Córdoba, both of which have provided facilities used for this study. M.L., C.U. are researchers from Argentine Council (CONICET) and K.R. from Agricultural Research Service (USDA). The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. IMIBIO-CONICET, Universidad Nacional de San Luis, 5700, San Luis, Argentina

    Mónica A. Lugo, Eugenia Menoyo & Esteban M. Crespo

  2. United States Department of Agriculture-Agricultural Research Service, Fort Keogh Livestock & Range Research Laboratory, 243 Fort Keogh Road, Miles City, MT, 59301-4016, USA

    Kurt O. Reinhart

  3. IMBIV-CONICET, Universidad Nacional de Córdoba, CC 495, 5000, Córdoba, Argentina

    Carlos Urcelay

Authors
  1. Mónica A. Lugo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kurt O. Reinhart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eugenia Menoyo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esteban M. Crespo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos Urcelay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mónica A. Lugo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Phylogeny (chronogram) of 42 plant species from Sierras de las Quijadas National Park (on the left) and percent arbuscular mycorrhizal root colonization. The phylogeny was created with the program Phylomatic with the R20120829 supertree. Circles indicate nodes with greater (●) or lower levels (○) of divergence than expected by chance (2-tailed test of significance, P ≤ 0.05). Families with two or more representative taxa are illustrated by vertical lines and family names. Branch tip numbers correspond to: 1 Ephedra sp., 2 Adesmia cordobensis, 3 A. aff. trijuga, 4 Monnina dictyocarpa, 5 Tricomaria usillo, 6 Larrea cuneifolia, 7 Bulnesia retama, 8 Plectrocarpa tetracantha, 9 Sida argentina, 10 Gomphrena colosacana var. andersonii, 11 Gomphrena pulchella subsp. rosea, 12 Atriplex argentina, 13 A. lampa, 14 A. lithophila, 15 A. quixadensis, 16 A. spegazzinii, 17 Opuntia sulphurea, 18 Tephrocactus articulatus, 19 Grahamia bracteata, 20 Portulaca confertifolia, 21 Halophyton ameghinoi, 22 Allionia incarnata, 23 Boerhavia pulchella, 24 Flavelia haumanii, 25 Thymophylla pentachaeta, 26 Trixis cacalioides, 27 Parthenium hysterophorus, 28 Senecio hualtaranensis, 29 Ehretia cortesia, 30 Cressa nudicaulis, 31 Evolvulus arizonicus, 32 Xeroaloysia ovatifolia, 33 Bromelia urbaniana, 34 Deuterocohnia longipetala, 35 Dyckia velascana, 36 Tillandsia angulosa, 37 T. xiphioides, 38 Aristida mendocina, 39 Pappophorum caespitosum, 40 Sporobolus phleoides, 41 Chloris castilloniana, 42 Setaria cordobensis (DOC 218 kb)

Fig. S2

Phylogeny (chronogram) of 42 plant species from Sierras de las Quijadas National Park (on the left) and percent rot colonization by dark septate endophytes. The phylogeny was created with the program Phylomatic with the R20120829 supertree. No nodes were determined to have greater or lower levels of divergence than expected by chance (2-tailed test of significance, P ≤ 0.05). Families with two or more representative taxa are illustrated by vertical lines and family names. Branch tip numbers correspond to: 1 Ephedra sp., 2 Adesmia cordobensis, 3 A. aff. trijuga, 4 Monnina dictyocarpa, 5 Tricomaria usillo, 6 Larrea cuneifolia, 7 Bulnesia retama, 8 Plectrocarpa tetracantha, 9 Sida argentina, 10 Gomphrena colosacana var. andersonii, 11 Gomphrena pulchella subsp. rosea, 12 Atriplex argentina, 13 A. lampa, 14 A. lithophila, 15 A. quixadensis, 16 A. spegazzinii, 17 Opuntia sulphurea, 18 Tephrocactus articulatus, 19 Grahamia bracteata, 20 Portulaca confertifolia, 21 Halophyton ameghinoi, 22 Allionia incarnata, 23 Boerhavia pulchella, 24 Flavelia haumanii, 25 Thymophylla pentachaeta, 26 Trixis cacalioides, 27 Parthenium hysterophorus, 28 Senecio hualtaranensis, 29 Ehretia cortesia, 30 Cressa nudicaulis, 31 Evolvulus arizonicus, 32 Xeroaloysia ovatifolia, 33 Bromelia urbaniana, 34 Deuterocohnia longipetala, 35 Dyckia velascana, 36 Tillandsia angulosa, 37 T. xiphioides, 38 Aristida mendocina, 39 Pappophorum caespitosum, 40 Sporobolus phleoides, 41 Chloris castilloniana, 42 Setaria cordobensis (DOC 217 kb)

Table S1

Studies that quantified the percent root colonization by arbuscular mycorrhizal fungi (AM) and dark septate endophytes (DSE) for 10 or more herbaceous plant species. Frequency of AM, DSEs and AM-DSE type colonization, AMF, DSEs root length colonization, and root fungal endophyte prevailing among different ecosystems and regions, considering mean annual precipitation (MAP) or total annual precipitation (TAP), altitude and soil features by plants species (DOC 61 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lugo, M.A., Reinhart, K.O., Menoyo, E. et al. Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment. Mycorrhiza 25, 85–95 (2015). https://doi.org/10.1007/s00572-014-0592-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-014-0592-5

Keywords

Search

Navigation