Abstract
Background
Volcanic activity alters earth surfaces creating environments where new ecosystems can be established. Just some plants are able to colonize this kind of environment. Low availability of nitrogen and phosphorus have been widely considered to restrict plant colonization on volcanic deposits worldwide. Root adaptations such as associations with mycorrhizal fungi, associations with nitrogen-fixing microorganisms, and root structures specialized to exude carboxylates, comprise mechanisms plants use to grow on low nutrient availability conditions, such as volcanic ash or tephra.
Scope
Most of the studies carried out on volcanic deposit colonizing plants have been focused on aboveground features such as plant survival, growth, and plant-plant interactions. Belowground processes, involving root activity and the rhizosphere, have been less studied. Plants that colonize different volcanically affected areas in the world, the effect on microorganisms associated mainly with the rhizosphere of these plants, microbe-microbe and microbe-plant interactions are reviewed here.
Conclusions
Plant-to-plant interactions, involving the different kind of roots adaptations, may be complementary to facilitate each other and positively influence the ecosystem recovery of volcanic deposits. At rhizosphere level, particular microbial communities can be recruited with specific beneficial functions (nitrogen-fixing, plant promoting growth, etc.) that improve soil development and plant colonization of volcanic deposits. New aspects such as the ability of mycorrhizal fungi to recruit bacteria able to solubilize phosphorus, and the presence of endophytes and their role in promoting the growth of early plant colonizers of volcanic are also discussed.
Similar content being viewed by others
References
Allard-Massicotte R, Tessier L, Lécuyer F, Lakshmanan V, Lucier JF, Garneau D et al (2016) Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. MBio 7. https://doi.org/10.1128/mBio.01664-16
Alberdi M, Reyes-Díaz M, Zúñiga R, Hess S, Bravo LA, Corcuera LJ (2009) Photochemical efficiency of PSII and photoprotective pigments in seedlings and adults of two Proteaceae with different shade tolerance from Chilean temperate rain forest. Rev Chil Hist Nat 82:387–402
Arnalds O (2013) The influence of volcanic tephra (ash) on ecosystems. Adv Agron 121:331–380
Ávila-Valdés A, Piper FI, Zúñiga-Feest A (2019) Cluster root formation and function vary in two species with contrasting geographic ranges. Plant Soil 440:25–38. https://doi.org/10.1007/s11104-019-04056-3
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Plant Biol 20:642–650
Baillie CK, Kaufholdt D, Karpinski LH, Schreiber V, Hänsch S, Evers C, Bloem E, Schnug E, Kreuzwieser J, Herschbach C, Rennenberg H, Mendel RR, Hänsch R (2016) Detoxification of volcanic sulfur surplus in planta: three different strategies of survival. Environ Exp Bot 126:44–56
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Buma B, Bisbing S, Krapek J, Wright G (2017) A foundation of ecology rediscovered: 100 years of succession on the William S. Cooper plots in Glacier Bay, Alaska. Ecology 98:1513–1523
Casanova-Katny MA, Torres-Mellado GA, Palfner G, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622
Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González S, Molina-Montenegro MA (2006) Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of Central Chile. New Phytol 169:59–69
Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S, Anthelme F, Björk RG, Dickinson KJM, Cranston BH, Gavilán R, Gutiérrez-Girón A, Kanka R, Maalouf JP, Mark AF, Noroozi J, Parajuli R, Phoenix GK, Reid AM, Ridenour WM, Rixen C, Wipf S, Zhao L, Escudero A, Zaitchik BF, Lingua E, Aschehoug ET, Callaway RM (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Lett 17:193–202
Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo JH, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430
Ciccazzo S, Esposito A, Rolli E, Zerbe S, Daffonchio D, Brusetti L (2014) Different pioneer plant species select specific rhizosphere bacterial communities in a high mountain environment. Springerplus 3:391
Dahlgren RA, Saigusa M, Ugolini FC (2004) The nature, properties and management of volcanic soils. Adv Agron 82:113–182
Dale VH, Campbell DR, Adams WM, Crisafulli CM, Dains VI, Frenzen PM, Holland RF (2005) Plant succession on the Mount St. Helens debris-avalanche deposit. In: Dale VH, Swanson FJ, Crisafulli CM (eds) Ecological responses to the 1980 eruptions of mount St. Helens. Springer-Verlag, New York, pp 59–73
de Ridder-Duine AS, Kowalchuk GA, Gunnewiek PJK, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357
del Moral R, Grishin SY (1999) Volcanic disturbances and ecosystem recovery. In: Walker RL (ed) Ecosystems of the world. Elsevier Science, Amsterdam, pp 137–160
del Moral R, Lacher IL (2005) Vegetation patterns 25 years after the eruption of Mount St. Helens, Washington, USA. Am J Bot 92:1948–1956
del Moral R, Rozzell LR (2005) Long-term effects of Lupinus lepidus on vegetation dynamics at Mount St. Helens. Plant Ecol 181:203–215
del Moral R, Wood DM, Titus JH (2005) Proximity, microsites, and biotic interactions during early succession. In: Dale VH, Swanson FJ, Crisafulli CM (eds) Ecological responses to the 1980 eruption of mount St. Helens. Springer, New York, pp 93–110
Delgado M, Suriyagoda L, Zúñiga-Feest A, Borie F, Lambers H, Field K (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
Delgado M, Zúñiga-Feest A, Almonacid L, Lambers H, Borie F (2015) Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil. Plant Soil 395:189–200
Deligne NI, Sigurdsson H (2015) Chapter 14 - Global Rates of Volcanism and Volcanic Episodes. In: Houghton B, McNutt S, Rymer H, Stix J (eds) Sigurdsson H. Academic Press, The Encyclopedia of Volcanoes (Second Edition), pp 265–272
el Zahar-Haichar F, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80
Feng H, Zhang N, Du W, Zhang H, Liu Y, Fu R et al (2018) Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant Microbe Interact 31:995–1005
Fiantis D, Ginting FI, Nelson M, Minasny B (2019) Volcanic ash, insecurity for the people but securing fertile soil for the future. Sustainability 11:3072. https://doi.org/10.3390/su11113072
Fujiyoshi M, Masuzawa T, Kagawa A, Nakatsubo T (2005) Successional changes in mycorrhizal type in the pioneer plant communities of a subalpine volcanic desert on Mt Fuji, Japan. Polar Biosci 18:60–72
Genre A, Lanfranco L, Perotto S, Bonfante P (2020) Unique and common traits in mycorrhizal symbioses. Nat Rev Microbiol 18:1–12. https://doi.org/10.1038/s41579-020-0402-3
Halvorson JJ, Smith JL (2008) Carbon and nitrogen accumulation and microbial activity in Mount St. Helens pyroclastic substrates after 25 years. Plant Soil 315:211–228
Hida A, Oku S, Kawasaki T, Nakashimada Y, Tajima T, Kato J (2015) Identification of the mcpA and mcpM genes, encoding methyl-accepting proteins involved in amino acid and l-malate chemotaxis, and involvement of McpM-mediated chemotaxis in plant infection by Ralstonia pseudosolanacearum (formerly Ralstonia solanacearum phylotypes I and III). Appl Environ Microbiol 81:7420–7430
Hurd T, Schwintzer C (1996) Formation of cluster roots in Alnus incana ssp. rugosa and other Alnus species. Can J Bot 74:684–1686
Ibekwe AM, Kennedy AC, Halvorson JJ, Yang C-H (2007) Characterization of developing microbial communities in Mount St. Helens pyroclastic substrate. Soil Biol Biochem 39:2496–2507
Jansa J, Bukovská P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts–or just soil free-riders? Front Plant Sci 4:134. https://doi.org/10.3389/fpls.2013.00134
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957
Jorquera MA, Hernández MT, Rengel Z, Marschner P, de la Luz Mora M (2008) Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil. Biol Fert Soil 44:1025–1034
Kandel SL, Joubert PM, Doty SL (2017) Bacterial Endophyte colonization and distribution within plants. Microorganisms 5:77. https://doi.org/10.3390/microorganisms5040077
Kikvidze Z, Armas C, Fukuda K, Martínez-García LB, Miyata M, Oda-Tanaka A, Pugnaire F I. Wu, B (2010) The role of arbuscular mycorrhizae in primary succession: differences and similarities across habitats. Web Ecol 10: 50–57
Kwon T, Tsuyuzaki S (2016) Differences in nitrogen redistribution between early and late plant colonizers through ectomycorrhizal fungi on the volcano mount Koma. Ecol Res 31:557–567
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evolut 23:95–103
Lambers H, Bishop JG, Hopper SD, Laliberte E, Zuniga-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
Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288
Lambers H, Nascimento DL, Oliveira RS, Shi J (2019) Do cluster roots of red alder play a role in nutrient acquisition from bedrock? Proc Natl Acad Sci U S A 116:11575–11576
Lamont BB, Pérez-Fernández M, Rodríguez-Sánchez J (2015) Soil bacteria hold the key to root cluster formation. New Phytol 206:1156–1162
Li L, Tilman D, Lambers H, Zhang F-Z (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69
Lozano YM, Hortal S, Armas C, Pugnaire FI (2014) Interactions among soil, plants, and microorganisms drive secondary succession in a dry environment. Soil Biol Biochem 78:298–306
Markham JH, Chanway CP (1999) Does past contact reduce the degree of mutualism in the Alnus rubra-Frankia symbiosis? Can J Bot 77:434–441
Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576
McIntire EJ, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201:403–416
Molina R, Myrold D, Li CY (1994) Root symbioses of red alder: technological opportunities for enhanced regeneration and soil improvement. In: Hibbs DE, De Bell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, Corvallis, OR, pp 23–46
Molina-Montenegro MA, Oses R, Torres-Díaz C, Atala C, Núñez MA, Armas C (2015) Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect Plant Ecol Evol Syst 17:218–226
Nara K (2006) Pioneer dwarf willow may facilitate tree succession by providing late colonizers with compatible ectomycorrhizal fungi in a primary successional volcanic desert. New Phytol 171:187–198
Nara K, Hogetsu T (2004) Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85:1700–1707
Nara K, Nakaya H, Hogetsu T (2003a) Ectomycorrhizal sporocarp succession and production during early primary succession on Mount Fuji. New Phytol 158:193–206
Nara K, Nakaya H, Wu BY, Zhou ZH, Hogetsu T (2003b) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159:743–756
Obase K, Tamai Y, Yajima T, Miyamoto T (2007) Mycorrhizal associations in woody plant species at the Mt Usu volcano, Japan. Mycorrhiza 17:209–215
Olivares E, Peña E, Aguiar G (2002) Metals and oxalate in Tithonia diversifolia (Asteraceae): concentrations in plants growing in contrasting soils, and Al induction of oxalate exudation by roots. J Plant Phys 159:743–749
Ordoñez YM, Fernandez BR, Lara LS, Rodriguez A, Uribe-Vélez D, Sanders IR (2016) Bacteria with phosphate solubilizing capacity alter mycorrhizal fungal growth both inside and outside the root and in the presence of native microbial communities. PloSOne 11:e0154438. https://doi.org/10.1371/journal.pone.0154438
Pfanzelt S, Jürke G, Rodríguez R (2008) A vegetation map of nevados de Chillan volcanic complex, Bio-Bio region, Chile. Gayana Bot 65:209–219
Piper FI, Baeza G, Zúñiga-Feest A, Fajardo A (2013) Soil nitrogen, and not phosphorus, promotes cluster-root formation in a south American Proteaceae. Am J Bot 100:2328–2338
Piper FI, Fajardo A, Baeza G, Cavieres L (2019) The association between a nurse cushion plant and a cluster-root bearing tree species alters the plant community structure. J Ecol 107:2182–2196
Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188-189:25–35
Rodríguez-Echeverría S, Lozano Y, Bardgett R (2016) Influence of soil microbiota in nurse plant systems. Funct Ecol 30:30–40
Roy J, Albert CH, Ibanez S, Saccone S, Zinger L, Choler P, Clément JC, Lavergne S, Geremia RA (2013) Microbes on the cliff: alpine cushion plants structure bacterial and fungal communities. Front Microbiol 4:64. https://doi.org/10.3389/fmicb.2013.00064
Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556
Sasse J, Martinoia E, Northen T (2018) Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Trends Plant Sci 23(1):25–41
Schwencke J, Carú M (2001) Advances in actinorhizal symbiosis: host plant-Frankia interactions, biology, and applications in arid land reclamation. A review. Arid Land Res Manag 15:285–327
Seeds JD, Bishop JG (2009) Low Frankia inoculation potentials in primary successional sites at Mount St. Helens, Washington, USA. Plant Soil 323:225–233
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125
Shehata HR, Dumigan C, Watts S, Raizada MN (2017) An endophytic microbe from an unusual volcanic swamp corn seeks and inhabits root hair cells to extract rock phosphate. Sci Rep 7:13479. https://doi.org/10.1038/s41598-017-14080-x
Shoji S, Takahashi T (2002) Environmental and agricultural significance of volcanic ash soils. Glob Environ Res 6:113–135
Stafford WHL, Baker GC, Brown SA, Burton SG, Cowan DA (2005) Bacterial diversity in the rhizosphere of Proteaceae species. Environ Microbiol 7:1755–1768
Titus JH, del Moral R (1998) Vesicular–arbuscular mycorrhizae influence mount St Helens pioneer species in greenhouse experiments. Oikos 81:495–510
Titus JH, Tsuyuzaki S (2003) Distribution of plants in relation to microsites on recent volcanic substrates on mount Koma, Hokkaido, Japan. Ecol Res 18:91–98
Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40:1971–1974
Tsuyuzaki S, Matsuda M, Akasaka M (2012) Effect of a deciduous shrub on microclimate along an elevation gradient, mount Koma, northern Japan. Clim Res 51:1–10
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15
Walker LR, del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, New York
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19
Wang Y, Lambers H (2020) Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives. Plant Soil 447(1):135–156
Wasaki J, Sakaguchi J, Yamamura T, Ito S, Shinano T, Osaki M, Kandeler E (2018) P and N deficiency change the relative abundance and function of rhizosphere microorganisms during cluster root development of white lupin (Lupinus albus L.). Soil Sci Plant Nutr 64:686–696
Weisskopf L, Heller S, Eberl L (2011) Burkholderia species are major inhabitants of white Lupin cluster roots. Appl Environ Microbiol 77:7715–7720
Wolters DJ, van Dijk C, Akkermans ADL, Woldendorp JW (1999) Ineffective Frankia and host resistance in natural populations of Alnus glutinosa (L.) Gaertn. Acta Oecol 20:71–79
Wu B, Isobe K, Ishii R (2004) Arbuscular mycorrhizal colonization of the dominant plant species in primary successional volcanic deserts on the southeast slope of Mount Fuji. Mycorrhiza 14:391–395
Wu B, Hogetsu T, Isobe K, Ishii R (2007) Community structure of arbuscular mycorrhizal fungi in a primary successional volcanic desert on the southeast slope of Mount Fuji. Mycorrhiza 17:495–506
Yoshitake S, Fujiyoshi M, Watanabe K, Masuzawa T, Nakatsubo T, Koizumi H (2013) Successional changes in the soil microbial community along a vegetation development sequence in a subalpine volcanic desert on Mount Fuji, Japan. Plant Soil 364:261–272
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME J 12:2339–2351
Zinger L, Lejon DP, Baptist F, Bouasria A, Aubert S, Geremia RA, Choler P (2011) Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoSOne 6:e19950. https://doi.org/10.1371/journal.pone.0019950
Zúñiga-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
Zúñiga-Feest A, Delgado M, Bustos A (2014) Cluster roots. In: Varma A (ed) Cluster roots. In: Morte A, Varma A (eds) Root engineering. Soil biology, vol 40. Springer, Berlin, Heidelberg, pp. 353–367
Zúñiga-Feest A, Delgado M, Bustos-Salazar A, Ochoa V (2015) The southern south American Proteaceae, Embothrium coccineum exhibits intraspecific variation in growth and cluster-root formation depending on climatic and edaphic origins. Plant Soil 396:201–213
Zúñiga-Feest A, Muñoz G, Bustos-Salazar A, Ramírez F, Delgado M, Valle S, Díaz L (2018) The nitrogen fixing specie Sophora cassioides (Fabaceae), is nutritionally favored and their rhizosphere bacteria modified when is cocultivated with the cluster root forming Embothrium coccineum (Proteaceae). J Soil Sci Plant Nutr 18:597–616
Acknowledgements
The authors thank the FONDECYT grants 1180669 and 1130440 for supporting our research, as well as Corporación Nacional Forestal de Chile (CONAF) for giving us access to protected areas affected by volcanic activity in Chile. Besides, the help of Karla Veas for making Fig. 2 is appreciated. Finally, authors also acknowledge the suggestions and comments of Dr. Hans Lambers and the anonymous referees for improving the manuscript at the different stages of this submission.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Stefano Cesco.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Muñoz, G., Orlando, J. & Zuñiga-Feest, A. Plants colonizing volcanic deposits: root adaptations and effects on rhizosphere microorganisms. Plant Soil 461, 265–279 (2021). https://doi.org/10.1007/s11104-020-04783-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04783-y