Arbuscular mycorrhizae and absence of cluster roots in the Brazilian Proteaceae Roupala montana Aubl.

Abstract

Plants growing on soils poor in phosphorus (P) develop P-acquisition strategies such as symbiotic associations with arbuscular mycorrhizal fungi (AMF). In very poor soils, cluster roots, a non-symbiotic alternative strategy enables plants to extract P uptake by developing modified roots. The latter strategy is characteristic (if not a derived trait) of the Southern Hemisphere Proteaceae, which are thus non-mycorrhizal. The Proteaceae have been studied mainly in Australia, where they are very diverse, especially on very P-poor soils. We investigated the presence of cluster roots and/or AMF in the Proteaceae Roupala montana Aubl. from three areas of the Brazilian Cerrado. This is, a seasonal neotropical savanna on highly weathered soils characterised by high aluminium content, low pH, and very low available P. We discovered that R. montana forms arbuscular mycorrhiza and no cluster roots were observed. All the plantlets collected were mycorrhizal. We also evaluated the fertility of the soil (especially the P availability). It was found that R. montana grows in soils containing more than 220 mg kg−1 total P. Thus, they are, more fertile than in most of Australian soils and likely have sufficient available P to support plant nutrition by way of mycorrhizae. Further research should investigate whether other Brazilian, and more generally non-Australian, Proteaceae species can establish associations with AMF, and the link with soil P availability. Our findings have implications for the phylogenetic patterns of loss of symbiosis with AMF within the Proteaceae.

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References

  1. Association of Official Analytical Chemistry - AOAC (1990) Official methods of analysis, 15th edn. AOAC International, Arlington

    Google Scholar 

  2. Barker NP, Weston PH, Rutschmann F, Sauquet H (2007) Molecular dating of the ‘Gondwanan’ plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. J Biogeogr 34:2012–2027

    Google Scholar 

  3. Bellgard SE (1991) Mycorrhizal associations of plant species in the Hawkesbury sandstone vegetation. Aust J Bot 39:357–364

    Google Scholar 

  4. Bononi VLR, Trufem SFT (1983) Endomicorrizas vesículo-arbusculares do cerrado da Reserva Biológica de Mogi-Guaçu, SP, Brasil. Rickia 10:55–84

    Google Scholar 

  5. Boulet FM, Lambers H (2005) Characterisation of arbuscular mycorrhizal fungi colonization in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultramafic soil. Plant Soil 269:357–367

    CAS  Google Scholar 

  6. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Google Scholar 

  7. 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

    CAS  Google Scholar 

  8. Brundrett MC (2017a) Distribution and evolution of mycorrhiza types and other specialised roots in Australia. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International, Cham, pp 361–394

    Google Scholar 

  9. Brundrett MC (2017b) Global diversity and importance of mycorrhiza and nonmycorrhizal plants. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International, Cham, pp 533–556

    Google Scholar 

  10. Campos ÉP, Duarte TG, Neri AV, Silva AF, Meira-Neto JAA, Valente GE (2006) Composição florística de um trecho de cerradão e cerrado sensu stricto e sua relação com o solo na floresta nacional (FLONA) de Paraopeba, MG, Brasil. Revista Árvore 30:471–479

    Google Scholar 

  11. Clesceri LS, Greenberg AE, Eaton AD (1998) Standard Methods for the Examination of Water and Wastewater. APHA, AWWA and WEF, Washington DC

    Google Scholar 

  12. Costa AA, Araújo GM (2001) Comparação da vegetação arbórea de cerradão e cerrado na Reserva do Panga, Uberlândia, Minas Gerais. Act Bot Bras 15:63–72

    Google Scholar 

  13. de Campos MCR (2011) Phosphorus-acquisition and phosphorus-conservation mechanisms of plants native to South-Western Australia or to Brazilian rupestrian fields, PhD thesis. In: The University of Western Australia

    Google Scholar 

  14. Delaux P-M, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané JM (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10:e1004487

    PubMed  PubMed Central  Google Scholar 

  15. Delgado M, Zúñiga-Feest A, Borie F, Suriyagoda L, Lambers H (2014) Divergent functioning of Proteaceae species: the south American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils. Funct Ecol 28:1356–1366

    Google Scholar 

  16. Detmann KSC, Rebello VPA, Leite TS, Delgado MN, Azevedo AA, Kasuya MCM, Almeida AM. (2007) Mycorrhization and nutritional status of Roupala montana (Proteaceae) in Cerrado. XI Conferência Brasileira de Fisiologia vegetal. Gramado-RS

  17. Detmann KSC, Delgado MN, Rebello VPA, Leite TS, Kasuya MCM, Azevedo AA, Almeida AM (2008) Fungos micorrízicos arbusculares e endofíticos do tipo dark septate em espécies nativas de cerrado. Rev Bras Ciênc Solo (Online) 32:1883–1890

    Google Scholar 

  18. Eiten G (1994) Vegetação do cerrado. In: Pinto MN (ed) Cerrado: caracterização, ocupação e perspectivas. Editora Universidade de Brasília, Brasília, pp 17–73

    Google Scholar 

  19. Franco AC (1998) Seasonal patterns of gas exchange, water relations and growth of Roupala montana, an evergreen savanna species. Plant Ecol 136:69–76

    Google Scholar 

  20. Franco AC, Bustamante M, Caldas LS, Goldstein G, Meinzer FC, Kozovits AR, Rundel P, Coradin VTR (2005) Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit. Trees 19:326–335

    Google Scholar 

  21. Güsewell S (2004) (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Google Scholar 

  22. Haridasan M (1992) Observations on soils, foliar nutrient concentrations and floristic composition of cerrado and cerradão communities in Central Brazil. In: Proctor J, Ratter JA, Furley PA (eds) The nature and dynamics of forest-savanna boundaries. Chapman and Hall, London, pp 171–184

    Google Scholar 

  23. Haridasan M (2008) Nutritional adaptations of native plants of the Cerrado biome in acid soils. Braz J Plant Physiol 20:183–195

    Google Scholar 

  24. Hoffmann WA (1998) Post-burn reproduction of woody plants in a neotropical savanna: the relative importance of sexual and vegetative reproduction. App Ecol 35:422–433

    Google Scholar 

  25. Hoot SB, Douglas AW (1998) Phylogeny of the Proteaceae based on atpB and atpB-rbcL intergenic spacer region sequences. Aust Syst Bot 11:301–320

    Google Scholar 

  26. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, YOung PW, Read DJ (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515

    Google Scholar 

  27. Kozovits AR, Bustamante MMC, Garofalo CR, Bucci S, Franco AC, Goldstein G, Meinzer FC (2007) Nutrient resorption and patterns of litter production and decomposition in a Neotropical savanna. Funct Ecol 21:1034–1043

    Google Scholar 

  28. Lambers H, Shane MW (2007) Role of root clusters in phosphorus acquisition and increasing biological diversity in agriculture. In: Spiertz JHJ, Struik PC, Van Laar HH (eds) Scale and complexity in plant systems research: Gene-Plant-crop relations. Springer, Dordrecht, pp 237–250

    Google Scholar 

  29. Lambers H, Teste FP (2013) Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient availability play the same game? Plant Cell Environ 36:1911–1915

    PubMed  Google Scholar 

  30. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    PubMed  PubMed Central  Google Scholar 

  31. Lambers H, Raven J, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Google Scholar 

  32. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    CAS  Google Scholar 

  33. Lambers H, Bishop JG, Hopper SD, Laliberté E, Zúñiga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110:329–348

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Lambers H, Clode PL, Hawkins H-J, Laliberté E, Oliveira R, Reddell P, Shane MW, Stitt M, Weston P (2015a) Metabolic adaptations of the non-mycotrophic Proteaceae to soil with a low phosphorus availability. In: Plaxton WC, Lambers H (eds) Phosphorus Metabolism in Plants, vol 48. John Wiley & Sons, pp 289–336

  35. Lambers H, Martinoia E, Renton M (2015b) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31

    CAS  PubMed  Google Scholar 

  36. Lamont BB (2003) Structure, ecology and physiology of root clusters–a review. Plant Soil 248:1–19

    CAS  Google Scholar 

  37. Mendonça RC, Felfini JM, Walter BMT, Silva MC, Rezende AV, Filgueiras TS, Nogueira PE (1998) Flora Vascular do Bioma Cerrado. In: Almeida SP (ed) Sano SM. Cerrado, Ambiente e Flora, Embrapa, Brazil, pp 289–556

    Google Scholar 

  38. Miller RM (2005) The nonmycorrhizal root – a strategy for survival in nutrient-impoverished soils. New Phytol 165:655–658

    PubMed  Google Scholar 

  39. Miller RM, Smith CR, Jastrow JD, Bever JD (1999) Mycorrhizal status of the genus Carex (Cyperaceae). Am J Bot 86:547–553

    CAS  PubMed  Google Scholar 

  40. Miranda JCC (2008) Cerrado: Micorriza Arbuscular - ocorrência e manejo. Embrapa Cerrados

  41. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Neri AV, Schaefer CEGR, Silva AF, Souza AL, Ferreira-Junior WG, Meira-Neto JAA (2012) The influence of soils on the floristic composition and community structure of an area of Brazilian Cerrado vegetation. Edinb J Bot 69:1–27

    Google Scholar 

  43. Neri AV, Schaefer CEGR, Souza AL, Ferreira-Junior WG, Meira-Neto JAA (2013) Pedology and plant physiognomies in the cerrado, Brazil. An Acad Bras Cienc 85:87–102

    CAS  PubMed  Google Scholar 

  44. O’Brien TP, Feder N, Mccully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

    Google Scholar 

  45. Obura PA (2008) Effect of soil properties on bioavailability of aluminium and phosphorus in selected Kenyan and Brazilian acid soils. PhD thesis, Purdue University, West Lafayette

    Google Scholar 

  46. Onstein RE, Jordan GJ, Sauquet H, Weston PH, Bouchenak-Khelladi Y, Carpenter RJ, Linder HP, Swenson N (2016) Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Glob Ecol Biogeogr 25:1239–1251

    Google Scholar 

  47. Pattinson GS, McGee PA (2004) Influence of colonisation by an arbuscular mycorrhizal fungus on the growth of seedlings of Banksia ericifolia (Proteaceae). Mycorrhiza 14:119–125

    CAS  PubMed  Google Scholar 

  48. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160

    Google Scholar 

  49. Piper FI, Baeza G, Zuñiga-Feest A, Fajardo A (2013) Soil nitrogen, and not phosphorus, promotes cluster-root formation in a south American Proteaceae, Embothrium coccineum. Am J Bot 100:2328–2338

    CAS  PubMed  Google Scholar 

  50. Pivello VR, Oliveras I, Miranda HS, Haridasan M, Sato MN, Meirelles ST (2010) Effect of fires on soil nutrient availability in an open savanna in Central Brazil. Plant Soil 337:111–123

    CAS  Google Scholar 

  51. Prance GT, Plana V (1998) The American Proteaceae. Aust Syst Bot 11:287–299

    Google Scholar 

  52. Rebelo T (1995) Sasol Proteas: A field guide to the proteas of Southern Africa. Fernwood Press, Vlaeberg

    Google Scholar 

  53. Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, Bothe H (2003) Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi. J Plant Physiol 160:615–626

    CAS  PubMed  Google Scholar 

  54. Resende JCF, Markewitz D, Klink CA, Bustamante MMC, Davidson EA (2011) Phosphorus cycling in a small watershed in the Brazilian Cerrado: impacts of frequent burning. Biogeochemistry 105:105–118

    CAS  Google Scholar 

  55. Selosse M-A, Le Tacon F (1998) The land flora: a phototroph–fungus partnership? Trends Ecol Evol 13:15–20

    CAS  PubMed  Google Scholar 

  56. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, Third edition. Amsterdam, the Netherlands. Academic Press

    Google Scholar 

  57. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, James TY (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Stock WD, Verboom GA (2012) Phylogenetic ecology of foliar N and P concentrations and N:P ratios across mediterranean-type ecosystems. Glob Ecol Biogeogr 21:1147–1156

    Google Scholar 

  59. Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534

    CAS  Google Scholar 

  60. Thomazini L (1974) Mycorrhiza in plants of the "Cerrado". Plant Soil 41:707–711

    Google Scholar 

  61. Tiessen H, Moir JO (2002) Characterisation of available P by sequential extraction. In: Carter MR (ed) Soil sampling and methods of analysis, 2nd edn. Canadian Society of Soil Science, Lewis Publishers, Boca Raton, Florida, pp 293–306

    Google Scholar 

  62. Trouvelot A, Kough J, Gianinazzi-Pearson V (1986) Evaluation of VA infection levels in root systems. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Research for estimation methods having a functional significance, Physiological and Genetical Aspects of Mycorrhizae. INRA Press, Paris, pp 217–221

    Google Scholar 

  63. van der Heijden MGA, Martin FM, Selosse MA, Sander IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    PubMed  Google Scholar 

  64. Van Reeuwijk LP (2002) Procedures for soil analysis. 6th ed. ISRIC, Wageningen.

  65. Veiga RS, Faccio A, Genre A, Pieterse CM, Bonfante P, van der Heijden MG (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937

    PubMed  Google Scholar 

  66. Villalobos-Vega R, Goldstein G, Haridasan M, Franco AC, Miralles-Wilhelm F, Scholz FG, Bucci SJ (2011) Leaf litter manipulations alter soil physicochemical properties and tree growth in a Neotropical savanna. Plant Soil 346:385–397

    CAS  Google Scholar 

  67. Weston PH (2007) Proteaceae. In: Kubitzki K (ed) The Families and Genera of VascularPlants IX Flowering Plants: Eudicots. Springer, Berlin-Heidelberg, pp 364–404

    Google Scholar 

  68. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Google Scholar 

  69. Zuñiga-Feest A, Delgado M, Alberdi M (2010) The effect of phosphorus on growth and cluster-root formation in the Chilean Proteaceae: Embothrium coccineum (R. et J. Forst.). Plant Soil 334:113–121

    Google Scholar 

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Acknowledgements

This research was supported by the following Brazilian agencies for financial support: the National Council of Scientific and Technological Development (CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico), the Minas Gerais Science Foundation (FAPEMIG - Fundação de Amparo à Pesquisa do Estado de Minas Gerais), and the Ecosocial Research Program of the Cerrado (PESCO – Programa de Pesquisas Ecossociais no Cerrado). Prof. João A. A. Meira-Neto and Gilmar E. Valente helped with plant material collection and identification. Nairam Felix de Barros and Roberta Boscaini Zandavalli critically read the manuscript. Edênio Detmann helped in the nutritional and statistical analysis. We also thank the Paraopeba National Forest Office (Instituto Chico Mendes de Conservação da Biodiversidade) for logistical support in the reserve used for this study, David Marsh for English correction and two anonymous referees for their detailed comments on this manuscript.

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Correspondence to Tiago de Souza Leite.

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Fig. S1

Cerrado vegetations present in the Paraopeba National Reserve, which correspond to the areas studied. Area 1: cerrado sensu stricto. Area 2: dense cerrado sensu stricto. Area 3: woodland savanna called dystrophic cerradão. (PDF 693 kb)

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da Silva Coutinho Detmann, K., de Souza Leite, T., de Oliveira Neto, R.R. et al. Arbuscular mycorrhizae and absence of cluster roots in the Brazilian Proteaceae Roupala montana Aubl.. Symbiosis 77, 115–122 (2019). https://doi.org/10.1007/s13199-018-0581-0

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Keywords

  • Arbuscular mycorrhiza
  • Cerrado
  • Cluster roots
  • Nutrient-acquisition strategy
  • phosphorus concentration