Trees

, Volume 28, Issue 4, pp 1021–1034 | Cite as

Responses of Senna reticulata, a legume tree from the Amazonian floodplains, to elevated atmospheric CO2 concentration and waterlogging

  • Bruna C. Arenque
  • Adriana Grandis
  • Olidan Pocius
  • Amanda P. de Souza
  • Marcos S. Buckeridge
Original Paper

Abstract

Key message

The Amazonian treeSenna reticulatashowed an increase in photosynthesis and starch content under elevated [CO2] that led an increment in biomass after 90 days. Elevated [CO2] was also capable of reducing the negative effect of waterlogging.

Abstract

Tree species from the Amazonian floodplains have to cope with low oxygen availability due to annual pulses of inundation that can last up to 7 months. Species capable of adapting to flooding and/or waterlogged conditions usually partition their storage to favor starch and allocate it to roots, where carbohydrates are used to maintain respiration rates during waterlogging. In spite of climate change, virtually nothing is known about how elevated atmospheric CO2 concentration ([CO2]) will affect plants when combined with waterlogging. In this work, we used open top chambers to evaluate the effect of elevated [CO2] during a period of terrestrial phase and in subsequent combination with waterlogged conditions to determine if the surplus carbon provided by elevated [CO2] may improve the waterlogging tolerance of the fast-growing Amazonian legume tree Senna reticulata. During the terrestrial phase, photosynthesis was ca. 28 % higher after 30, 45 and 120 days of elevated [CO2], and starch content in the leaves was, on average, 49 % higher than with ambient [CO2]. Total biomass was inversely correlated to the starch content of leaves, indicating that starch might be the main carbohydrate source for biomass production during the terrestrial phase. This response was more pronounced under elevated [CO2], resulting in 30 % more biomass in comparison to ambient [CO2] plants. After 135 days at elevated [CO2] an inversion has been observed in total biomass accumulation, in which ambient [CO2] presented a greater increment in total biomass in comparison to elevated [CO2], indicating negative effects on growth after long-term CO2 exposure. However, plants with elevated [CO2]/waterlogged displayed a greater increment in biomass in comparison with ambient [CO2]/waterlogged that, unlike during the terrestrial phase, was unrelated to starch reserves. We conclude that S. reticulata displays mechanisms that make this species capable of responding positively to elevated [CO2] during the first pulse of growth. This response capacity is also associated with a “buffering effect” that prevents the plants from decreasing their biomass under waterlogged conditions.

Keywords

High CO2 Flooding Starch Waterlogging Carbohydrates Amazon Senna reticulata Climate Change 

References

  1. Amaral LIV, Gaspar M, Costa PMF, Aidar MPM, Buckeridge MS (2007) Novo método enzimático rápido e sensível de extração e dosagem de amido em materiais vegetais. Hoehnea 34:425–431CrossRefGoogle Scholar
  2. Armstrong W, Brändle R, Jackson MB (1994) Mechanisms of flood tolerance in plants. Acta Botanica Neerlandica 43:307–358CrossRefGoogle Scholar
  3. Arpagaus S, Braendle R (2000) The significance of alfa-amilase under anoxia stress in tolerant rhizomes (Acorus calamus L.) and nontolerant tubers (Solanum tuberosum L.) var. Désirée. J Exp Bot 51:1475–1477PubMedCrossRefGoogle Scholar
  4. Baettig MB, Wild M, Imboden DM (2007) A climate change index: where climate change may be most prominent in the 21st century. Geophys Res Lett 34:L01705Google Scholar
  5. Braendle R (1991) Flooding resistance of rhizomatous amphibious plants. In: Jackson MB, Davies DD, Lambers H (eds) Plant life under oxygen stress: ecology, physiology and biochemistry. Academic Publishing, The Hague, pp 35–46Google Scholar
  6. Castonguay Y, Nadeau P, Simard R (1993) Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa. Plant Cell Environ 16:695–702CrossRefGoogle Scholar
  7. Centritto M, Lee HSJ, Jarvis PG (1999) Increased growth in elevated [CO2]: an early, short-term response? Glob Change Biol 5:623–633CrossRefGoogle Scholar
  8. Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  9. Davies FS, Flore JA (1986) Flooding, gas exchange and hydraulic conductivity of highbush blueberry. Physiol Plant 67:545–551CrossRefGoogle Scholar
  10. De Souza AP, Gaspar M, da Silva EA et al (2008) Elevated CO2 increases photosynthesis, biomass and productivity, and modifies gene expression in sugarcane. Plant Cell Environ 31:1116–1127PubMedCrossRefGoogle Scholar
  11. Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefGoogle Scholar
  12. Drew MC, Bazzaz FA (1978) Variation in distribution of assimilates among plant parts in three populations of Populus deltoides. Silvae Genetica 27:189–193Google Scholar
  13. Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New YorkGoogle Scholar
  14. Ferreira CS, Piedade MTF, Tine MAS, Rossatto DR, Parolin P, Buckeridge MS (2009) The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded. Ann Bot 104:1111–1119CrossRefGoogle Scholar
  15. Gonçalves JFC, Barreto DCS, Santos UM Jr, Fernandes AV, Sampaio PTB, Buckeridge MS (2005) Growth, photosynthesis and stress indicators in young rosewood plants (Aniba rosaeodora Duck) under different light intensities. Braz J Plant Physiol 17:325–334Google Scholar
  16. Gonçalves JFC, Lim RBS, Fernandes AV, Borges EELB, Buckeridge MS (2010) Physiological and biochemical characterization of the assai palm (Euterpe oleracea MART.) during seed germination and seedling growth under aerobic and anaerobic conditions. Revista Árvore 34:1045–1054CrossRefGoogle Scholar
  17. Gravatt DA, Kirby CJ (1998) Patterns of photosynthesis and starch allocation in seedlings of four bottom land hardwood tree species subjected to flooding. Tree Physiol 18:411–417PubMedCrossRefGoogle Scholar
  18. Guglielminetti L, Perata P, Alpi A (1995) Effect of anoxia on carbohydrate metabolism in rice seedlings. Plant Physiol 108:735–741PubMedCentralPubMedGoogle Scholar
  19. Junk WJ (1989) Flood tolerance and tree distribution in Central Amazonian floodplains. In: Nielsen LB, Nielsen IC, Balslev H (eds) Tropical forests: botanical dynamics, speciation and diversity. Academic Press, London, pp 47–64Google Scholar
  20. Junk WJ (1993) Wetlands of tropical South-America. In: Whigham D, Hejny S, Dykyjova D (eds) Wetlands of the world. Kluve, Dordrecht, pp 679–739Google Scholar
  21. Kerstiens G, Hawes C (1994) Response of growth and carbon allocation to elevated CO2 in young cherry (Prunus avium L.) saplings in relation to root environment. New Phytol 128:607–614CrossRefGoogle Scholar
  22. Körner C (2009) Responses of humid tropical trees to rising CO2. Annu Rev Ecol Evol Syst 40:61–79CrossRefGoogle Scholar
  23. Körner C, Miglietta F (1994) Long-term effects of naturally elevated CO2 on mediterranean grassland and forest trees. Oecologia 99:343–351CrossRefGoogle Scholar
  24. Körner C, Pelaez-Riedl S, Van Bel AJE (1995) CO2 responsiveness of plants: a possible link to phloem loading. Plant Cell Environ 18:595–600CrossRefGoogle Scholar
  25. Kreuzwieser J, Papadopoulou E, Rennenberg H (2004) Interaction of flooding with carbon metabolism of forest trees. Plant Biol 6:299–306PubMedCrossRefGoogle Scholar
  26. Lambers H, Poorter H (2004) Inherent variation in growth rate between higher plant: a search for physiological causes and ecological consequences. Adv Ecol Res 34:283–362CrossRefGoogle Scholar
  27. Leakey ADB, Bernacchi CJ, Ort DR, Long SP (2006) Long-term growth of soybean at elevated [CO2] does not cause acclimation of stomatal conductance under fully open-air conditions. Plant Cell Environ 29:1794–1800PubMedCrossRefGoogle Scholar
  28. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the Future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  29. Ludewig F, Sonnewald U, Kauder F, Heineke D, Geiger M, Stitt M, Mullerrober BT, Gillissen B, Kuhn C, Frommer WB (1998) The role of transient starch in acclimation to elevated atmospheric CO2. FEBS Lett 429:147–151PubMedCrossRefGoogle Scholar
  30. Luo Y, Chen JL, Reynolds JF, Field CB, Mooney HA (1997) Disproportional increases in photosynthesis and plant biomass in a Californian grassland exposed to elevated CO2: a simulation analysis. Funct Ecol 11:696–704CrossRefGoogle Scholar
  31. Marengo JA, Nobre CA, Sampaio G, Salazar LF, Borma LS (2011) Climate change in the Amazon Basin: tipping points, changes in extremes and impacts on natural and human system. In: Bush M, Flenley J, Gosling W (eds) Tropical rainforest responses to climate change, 2nd edn. Springer, Berlin, pp 259–278CrossRefGoogle Scholar
  32. Medina CL, Sanches MC, Tucci MLS, Sousa CAF, Cuzzuol GRF, Joly CA (2009) Erythrina speciosa (Leguminosae-Papilionoideae) under soil water saturation: morphophysiological and growth responses. Ann Bot 104:671–680PubMedCentralPubMedCrossRefGoogle Scholar
  33. Megonigal JP, Vann CD, Wolf AA (2005) Flooding constraints on tree (Taxodium distichum) and herb growth responses to elevated CO2. Wetlands 25:430–438CrossRefGoogle Scholar
  34. Mielke MS, Almeida AF, Gomes FP, Aguilar MAG, Mangabeira PAO (2003) Leaf gas exchange, chlorophyll fluorescence and growth responses of Genipa americana seedlings to soil flooding. Environ Exp Bot 50:221–231CrossRefGoogle Scholar
  35. Paez A, Hellmers H, Strain BR (1984) Carbon dioxide enrichment and water stress interaction on growth of two tomato cultivars. J Agric Sci 102:687–693CrossRefGoogle Scholar
  36. Parolin P (1997) Auswirkungen periodischer Vernässung und Überflutung auf Phänologie, Photosynthese und Blattphysiologie von Baumarten unterschiedlicher Wachstumsstrategie in zentralamazonischen Überschwemmungsgebieten. Herbert Utz Verlag Wissenschaft, MunichGoogle Scholar
  37. Parolin P (2001) Senna reticulata, a pioneer tree from Amazonian várzea floodplains. Bot Rev 67:239–254CrossRefGoogle Scholar
  38. Parolin P (2009) Drought responses of flood-tolerant Amazonian trees. Ann Bot 103:359–376PubMedCentralPubMedCrossRefGoogle Scholar
  39. Parolin P, De Simone O, Haase K, Waldhoff D, Rottenberger S, Kuhn U, Kesselmeier J, Kleiss B, Schmidt W, Pledade MTF, Junk WJ (2004) Central Amazonian floodplain forests: tree adaptations in a pulsing system. Bot Rev 70(3):357–380CrossRefGoogle Scholar
  40. Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312CrossRefGoogle Scholar
  41. Poorter H (1989) Interspecific variation in relative growth rate: on ecological causes and physiological consequences. In: Lambers H (ed) Causes and consequences of variation in growth rate. SPB Academic Publishing, The Hague, pp 45–68Google Scholar
  42. Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607CrossRefGoogle Scholar
  43. Poorter H, Pérez-Soba M (2002) Plant growth at elevated CO2. In: Mooney HA, Canadell JG (eds) The earth system: biological and ecological dimensions of global environmental change. Encyclopedia of global environmental change, vol 2. Wiley, Chichester, pp 489–496Google Scholar
  44. Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol 94:621–627PubMedCentralPubMedCrossRefGoogle Scholar
  45. Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012a) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850CrossRefGoogle Scholar
  46. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012b) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50PubMedCrossRefGoogle Scholar
  47. Rasinini GK, Guha A, Reddy AR (2011) Responses of Gmelina arborea, a tropical deciduous tree species, to elevated atmospheric CO2: growth, biomass productivity and carbon sequestration efficacy. Plant Sci 181:428–438CrossRefGoogle Scholar
  48. Rasse DP, Tocquin P (2006) Leaf carbohydrate controls over Arabidopsis growth and response to elevated CO2: an experimentally based model. New Phytol 172:500–513PubMedCrossRefGoogle Scholar
  49. Rasse DP, Peresta G, Drake BG (2005) Seventeen years of elevated CO2 exposure in a Chesapeake Bay Wetland: sustained but contrasting responses of plant growth and CO2 uptake. Glob Change Biol 11:369–377CrossRefGoogle Scholar
  50. Sage R (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynth Res 39:351–368PubMedCrossRefGoogle Scholar
  51. Scarano FR, Crawford RMM (1992) Ontogeny and the concept of anoxia-tolerance: the case of the Amazonian leguminous tree Parkia pendula. J Trop Ecol 8:349–352CrossRefGoogle Scholar
  52. Scarano FB, Cattânio JH, Crawford RMM (1994) Root carbohydrate storage in young saplings of Amazonian tidal várzea forest before the onset of the wet season. Acta Botanica Brasilica 8:129–139Google Scholar
  53. Scarano FR, Ribeiro KT, Moraes LFD, Lima HC (1997) Plant establishment on flooded and un-flooded patches of a freshwater swamp forest in southeastern Brazil. J Trop Ecol 14:793–803CrossRefGoogle Scholar
  54. Schlüter U, Crawford RMM (2001) Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. J Exp Bot 52:2213–2225PubMedGoogle Scholar
  55. Sij JW, Swanson CA (1973) Effects of petiole anoxia on phloem transport in squash. Plant Physiol 51:368–371PubMedCentralPubMedCrossRefGoogle Scholar
  56. Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14:741–762CrossRefGoogle Scholar
  57. Vergara W, Scholz SM (2011) Assessment of the risk of Amazon Dieback. The World Bank, Washington, DCGoogle Scholar
  58. Wong S (1990) Elevated atmospheric partial pressure of CO2 and plant growth. Non-structural carbohydrate content in cotton plants and its effect on growth parameters. Photosynth Res 23:171–180PubMedCrossRefGoogle Scholar
  59. Wray SM, Strain BR (1986) Response of two old field perennials to interactions of CO2 enrichment and drought stress. Am J Bot 73:1486–1491CrossRefGoogle Scholar
  60. Zimmermann MH (1971) Storage, mobilization and circulation of assimilates. In: Zimmermann MH, Brown CL (eds) Trees: structure and function. Springer, New York, pp 307–322CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Bruna C. Arenque
    • 1
  • Adriana Grandis
    • 1
  • Olidan Pocius
    • 2
  • Amanda P. de Souza
    • 1
  • Marcos S. Buckeridge
    • 1
  1. 1.Laboratório de Fisiologia Ecológica de Plantas (LAFIECO), Departamento de BotânicaInstituto de Biociências da Universidade de São PauloSão PauloBrazil
  2. 2.Laboratório de Fisioecologia, Departamento de EcologiaInstituto de Biociências da Universidade de São PauloSão PauloBrazil

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