Adaptations of Central Amazon Tree Species to Prolonged Flooding: Root Morphology and Leaf Longevity

Abstract

Várzeas are species-rich forest communities of the Central Amazon floodplains, inhabited by highly adapted tree species that can withstand long flooding periods. The leaf shedding behaviour and morphological traits that may contribute to adaptation to low oxygen levels were studied at the Ilha de Marchantaria on the lower Solimões-Amazonas river, Brazil, and in greenhouse experiments with cuttings of six tree species typical of the Amazon floodplain. Comparison of deciduousness in situ revealed that four of the species under investigation, Salix martiana, Tabernaemontana juruana, Laetia corymbulosa and Pouteria glomerata, are able to maintain their leaf system during the aquatic period. Adventitious roots were formed by S. martiana and T. juruana, but anatomical characteristics differed between the species. Whereas S. martiana developed lysigenous aerenchyma in its roots during aerobic and anaerobic growth, only small intercellular spaces of schizogenous origin were formed in the root cortex of T. juruana. Similar to the latter species, such spaces were constitutively formed in the deciduous species Crateva benthami and Vitex cymosa. Suberin deposits were observed in tangential and radial cell walls of the hypodermis of roots from T. juruana, L. corymbulosa and P. glomerata. Suberin deposits were less pronounced in roots of S. martiana and absent in V. cymosa and C. benthami. The data show that different, almost contrasting, survival mechanisms have evolved in roots of plants with similar life forms in the same habitat. The results further suggest that the morphological traits of the investigated trees are causally linked with the in situ leaf shedding behaviour.

Key words

Aerenchyma - adventitious roots - Central Amazon floodplain - inundation forest - oxygen distribution - suberin - soil flooding

References

• 1 Armstrong,  J.,, Armstrong,  W.,, and Beckett,  M. P.. (1992);  Phragmites australis: venturi- and humidity-induced pressure flows enhance rhizome aeration and rhizosphere oxidation.  New Phytologist. 120 197-207
• 2 Armstrong,  W., and Beckett,  P. M.. (1987);  Internal aeration and the development of stelar anoxia in submerged roots: a multishelled mathematical model combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers, and the rhizosphere.  New Phytologist. 105 221-245
• 3 Armstrong,  W.,, Brändle,  R.,, and Jackson,  M. B.. (1994);  Mechanisms of flood tolerance in plants.  Acta Botanica Neerlandica. 43 307-358
• 4 Armstrong,  W.,, Cousins,  D.,, Armstrong,  J.,, Turner,  D. W.,, and Beckett,  P. M.. (2000);  Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis.  Annals of Botany. 86 687-703
• 5 Begg,  C. B. M.,, Kirk,  G. J. D.,, MacKenzie,  A. F.,, and Neue,  H.-U.. (1994);  Root-induced iron oxidation and pH changes in the lowland rice rhizosphere.  New Phytologist. 128 469-477
• 6 Blom,  C. W. P. M.,, Voeseneck,  L. A. C. J.,, Banga,  M.,, Engelaar,  W.,, Rijnders,  J.,, Steeg,  H. V. D.,, and Visser,  E.. (1994);  Physiological ecology of riverside species: adaptive responses of plants to submergence.  Annals of Botany. 74 253-263
• 7 Chang,  C., and Shockey,  J. A.. (1999);  The ethylene-response pathway: signal perception to gene regulation.  Current Opinion in Plant Biology. 2 352-358
• 8 Christensen,  P. B.,, Revsbech,  N. P.,, and Sand-Jensen,  K.. (1994);  Microsensor analysis of oxygen in the rhizosphere of the aquatic macrophyte Lttorella uniflora (L.) Ascherson.  Plant Physiology. 105 847-852
• 9 Collmer,  T. D.,, Gibberd,  M. R.,, Wiengweera,  A.,, and Tinh,  T. K.. (1998);  The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant nutrient solution.  Journal of Experimental Botany. 49 1431-1436
• 10 Drew,  M. C., and Lynch,  J. M.. (1980);  Soil anaerobiosis, microorganisms, and root function.  Annual Review of Phytopathology. 18 37-66
• 11 Drew,  M. C.,, He,  C.-J.,, and Morgan,  P. W.. (2000);  Programmed cell death and aerenchyma formation in roots.  Trends In Plant Science. 5 123-127
• 12 Gill,  C.. (1975);  The ecological significance of adventitious rooting as a response to flooding in woody species, with special reference to Alnus glutinosa (L.) Gaertn.  Flora . 164 85-97
• 13 Gottsberger,  G.. (1978);  Seed dispersal by fish in the inundated regions of Humaitá, Amazonia.  Biotropica. 10 170-183
• 14 Goulding,  M.. (1980) The fishes and the forest: explorations in Amazonia natural history. Berkeley; California University Press
• 15 Gunawardena,  A. H. L. A. N.,, Pearce,  D. M.,, Jackson,  M. B.,, Hawes,  C. R.,, and Evans,  D. E.. (2001);  Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).  Planta. 212 205-214
• 16 He,  C.-J.,, Morgan,  P. W.,, and Drew,  M. C.. (1996);  Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia.  Plant Physiology. 112 463-472
• 17 Jackson,  M. B., and Armstrong,  W.. (1999);  Formation of aerenchyma and the process of plant ventilation to soil flooding and submergence.  Plant Biology. 1 274-287
• 18 Joly,  C. A., and Crawford,  R. M. M.. (1982);  Variation in tolerance and metabolic responses to flooding in some tropical trees.  Journal of Experimental Botany. 33 799-809
• 19 Junk,  W. J.. (1997) Distribution and size of neotropical floodplains. The Central Amazon floodplain Ecological Studies 126. Junk, W.J., ed. Berlin; Springer 12-16
• 20 Justin,  S. H. F. W., and Armstrong,  W.. (1991);  Evidence for the involvement of ethene in aerenchyma formation of adventitious roots of rice (Oryza sativa L.).  New Phytologist. 118 49-62
• 21 Kozlowski,  T. T.. (1984);  Plant responses to flooding of soil.  Bioscience. 34 162-167
• 22 Kozlowski,  T. T.. (1997);  Responses of woody plants to flooding and salinity.  Tree Physiology Monograph. 1 1-29
• 23 Lulai,  E. C., and Morgan,  M. C.. (1992);  Histochemical probing of potato periderm with neutral red: a sensitive cytofluorochrome for the hydrophobic domain of suberin.  Biotechnic and Histochemistry. 67 185-195
• 24 Parolin,  P.. (2001);  Seed germination of early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains.  Aquatic Botany. 70 89-103
• 25 Pavelic,  D.,, Arpagaus,  S.,, Rawyler,  A.,, and Brändle,  R.. (2000);  Impact of post-anoxia stress on the membrane lipids of anoxia-pretreated potato cells. A re-appraisal.  Plant Physiology. 124 1285-1292
• 26 Prance,  G. T.. (1979);  Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subjected to inundation.  Brittonia. 31 26-38
• 27 Saab,  N., and Sachs,  M. M.. (1996);  A flooding induced xyloglucan endo-transglycosylase in maize is responsive to ethylene and associated with aerenchyma.  Plant Physiology. 112 385-391
• 28 Saleque,  M. A., and Kirk,  G. J. D.. (1995);  Root-induced solubilization of phosphate in the rhizosphere of lowland rice.  New Phytologist. 129 325-336
• 29 Seago,  J. L.,, Peterson,  C. A.,, and Enstone,  D. E.. (2000);  Cortical development in roots of the aquatic plant Pontederia cordata (Pontederiaceae).  American Journal of Botany. 87 1116-1127
• 30 Sioli,  H.. (1968);  Hydrochemistry and geology in the Brasilian Amazon region.  Amazoniana. 1 267-277
• 31 Smirnoff,  N., and Crawford,  R. M. M.. (1983);  Variation in the structure and response to flooding of root aerenchyma in some wetland plants.  Annals of Botany. 51 237-249
• 32 Sorrell,  B.. (1994);  Airspace structure and mathematical modelling of oxygen diffusion, aeration, and anoxia in Elocharis sphacelata R. Br. roots.  Australian Journal of Marine Freshwater Research. 45 1529-1541
• 33 Visser,  E.,, Blom,  C. W. P. M.,, and Voesenek,  L. A. C. J.. (1996);  Flooding-induced adventitious rooting in Rumex: morphology and development in an ecological perspective.  Acta Botanica Neerlandica. 45 17-28
• 34 Visser,  E.,, Abben,  R.,, Blom,  C. W. P. M.,, and Voesenek,  L. A. C. J.. (1997);  Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations.  Plant, Cell and Environment. 20 647-653
• 35 Vriezen,  W. H.,, van Rijn,  C. P. E.,, Voesenek,  L. A. C. J.,, and Mariani,  C.. (1997);  A homolog of the Arabidopsis thaliana ERS gene is actively regulated in Rumex palustris upon flooding.  The Plant Journal. 11 1265-1271
• 36 Waldhoff,  D.,, Junk,  W. J.,, and Furch,  B.. (1998);  Responses of three Central Amazonian tree species to drought and flooding under controlled conditions.  International Journal of Ecology and Environmental Sciences. 24 237-252
• 37 Wang,  T., and Peverly,  J. H.. (1999);  Iron oxidation states on root surfaces of a wetland plant (Phragmites australis).  Soil Science Society of America Journal. 63 247-252
• 38 Worbes,  M.. (1985);  Structural and other adaptations to long-term flooding by trees in Central Amazonia.  Amazoniana. 9 459-484
• 39 Worbes,  M.,, Klinge,  H.,, Revilla,  J. D.,, and Martius,  C.. (1992);  On the dynamics, floristic subdivision and geographical distribution of várzea forests in Central Amazonia.  Journal of Vegetation Science. 3 553-564
• 40 Yamamoto,  F.,, Sakata,  T.,, and Terazawa,  K.. (1995);  Physiological, morphological and anatomical responses of Fraxinus mandshurica seedlings to flooding.  Tree Physiology. 15 713-719

Section Editor: L. A. C. J. Voesenek