Abstract
Context
In response to waterlogging, pedunculate oak is known to develop adventitious roots and hypertrophied lenticels. However, to date, a link between these adaptations and the ability to maintain net CO2 assimilation rates and growth has not been demonstrated.
Aims
The aim of this study was to explore the cause–effect relationship between the ability to form morphological adaptations (hypertrophied lenticels and adventitious roots) and the capacity to maintain high assimilation rate and growth.
Methods
The occurrence of morphological adaptations and the parameters of photosynthesis were monitored over 20 days of waterlogging in 5-week-old pedunculate oak seedlings presenting similar morphological development.
Results
Based on the development or not of morphological adaptations, the following three categories of responses were identified: development of hypertrophied lenticels and adventitious roots, development of hypertrophied lenticels alone, and the lack of development of adaptive structures. These categories, ranked in the order given, corresponded to decreasing levels of initial net CO2 assimilation rate growth and photosynthesis parameters observed during waterlogging.
Conclusion
We observed a two-way cause–effect relationship between the capacity to form adaptive structures and the assimilation rate. Indeed, the initial assimilation rate determined the occurrence of hypertrophied lenticels and growth during stress, and then the development of morphological adaptations enhanced the ability to maintain assimilation levels during the stress.
Similar content being viewed by others
References
Calvo-Polanco M, Señorans J, Zwiazek JJ (2012) Role of adventitious roots in water relations of tamarack (Larix laricina) seedlings exposed to flooding. BMC Plant Biol 12:99–108. doi:https://doi.org/10.1186/1471-2229-12-99
Copolovici L, Niinemets U (2010) Flooding induced emissions of volatile signaling compounds in three tree species with differing waterlogging tolerance. Plant Cell Environ 33:1582–1594. doi:https://doi.org/10.1111/j.1365-3040.2010.02166.x
de Oliveira V, Joly C (2010) Flooding tolerance of Calophyllum brasiliense Camb. (Clusiaceae): morphological, physiological and growth responses. Trees Struct Funct 24:185–193. doi:https://doi.org/10.1007/s00468-009-0392-2
Dittert K, Wotzel J, Sattelmacher B (2006) Responses of Alnus glutinosa to anaerobic conditions—mechanisms and rate of oxygen flux into the roots. Plant Biol 8:212–223. doi:https://doi.org/10.1055/s-2005-873041
Dreyer E (1994) Compared sensitivity of seedlings from 3 woody species (Quercus robur L., Quercus rubra L., and Fagus sylvatica L.) to water-logging and associated root hypoxia: effects on water relations and photosynthesis. Ann For Sci 51:417–429. doi:https://doi.org/10.1051/forest:19940407
Du KB, Shen BX, Xu L, Tu BK (2008) Estimation of genetic variances in flood tolerance of poplar and selection of resistant F1 generations. Agrofor Syst 74:243–257. doi:https://doi.org/10.1007/s10457-008-9112-y
Ferner E, Renneberg H, Kreuzwieser J (2012) Effect of flooding on C metabolism of flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree Physiol 32:135–145. doi:https://doi.org/10.1093/treephys/tps009
Folzer H, Dat JF, Capelli N, Rieffel D, Badot PM (2006) Response of sessile oak seedlings (Quercus petraea) to flooding: an integrated study. Tree Physiol 26:759–766. doi:https://doi.org/10.1093/treephys/26.6.759
Gravatt DA, Kirby CJ (1998) Patterns of photosynthesis and starch allocation in seedlings of four bottomland hardwood tree species subjected to flooding. Tree Physiol 18:411–417. doi:https://doi.org/10.1093/treephys/18.6.411
Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol Monogr 1:1–29
Kreuzwieser J, Papadopoulou E, Rennenberg H (2004) Interaction of flooding with carbon metabolism of forest trees. Plant Biol 6:299–306. doi:https://doi.org/10.1055/s-2004-817882
Larson D, Davies FS, Schaffer B (1991) Floodwater temperature and stem lenticel hypertrophy in Mangifera indica (Anacardiaceae). Am J Bot 78:1397–1403. doi:https://doi.org/10.2307/2445278
Lévy G, Lefèvre Y, Becker M, Frochot LH, Picard JF, Wagner PA (1999) Excess water: effects on growth of the oak tree. Rev For Fr 51:151–161. doi:https://doi.org/10.4267/2042/5427
Mielke MS, De Almeida AAF, 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 50:221–231. doi:https://doi.org/10.1007/s11738-010-0702-8
Parelle J, Brendel O, Bodenes C, Berveiller D, Dizengremel P, Jolivet Y, Dreyer E (2006) Differences in morphological and physiological responses to water-logging between two sympatric oak species (Quercus petraea [Matt.] Liebl., Quercus robur L.). Ann For Sci 63:849–859. doi:https://doi.org/10.1051/forest:2006068
Parelle J, Brendel O, Jolivet Y, Dreyer E (2007) Intra and inter-specific diversity of the response to water-logging in two co-occuring white oak species (Quercus robur and Q. petraea). Tree Physiol 27:1027–1034. doi:https://doi.org/10.1093/treephys/27.7.1027
Parent C, Crèvecoeur M, Capelli N, Dat JF (2011) Contrasting and adaptive responses of two oak species to flooding stress: role of non-synbiotic haemoglobin. Plant Cell Environ 34:1113–1126. doi:https://doi.org/10.1111/j.1365-3040.2011.02309.x
Pezeshki SR, Pardue JH, DeLaune RD (1996) Leaf gas exchange and growth of flood-tolerant and flood-sensitive tree species under low soil redox conditions. Tree Physiol 16:453–458. doi:https://doi.org/10.1093/treephys/16.4.453
R Development Core Team (2012) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna (http://www.R-project.org)
Schmull M, Thomas FM (2000) Morphological and physiological reactions of young deciduous trees (Quercus robur L., Q. petraea [Matt.] Liebl., Fagus sylvatica L.) to waterlogging. Plant Soil 225:227–242. doi:https://doi.org/10.1023/A:1026516027096
Sena Gomes AR, Kozlowski TT (1980) Growth responses and adaptations of Fraxinus pennsylvanica seedlings to flooding. Plant Physiol 66:267–271. doi:https://doi.org/10.1104/pp. 66.2.267
Shimamura S, Yamamoto R, Nakamura T, Shimada S, Komatsu S (2010) Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Ann Bot 106:277–284. doi:https://doi.org/10.1093/aob/mcq123
Tang ZC, Kozlowski TT (1984) Water relations, ethylene production, and morphological adaptation of Fraxinus pennsylvanica seedlings to flooding. Plant Soil 77:183–192. doi:https://doi.org/10.1007/BF02182922
Wagner P, Dreyer E (1997) Interactive effects of waterlogging and irradiance on the photosynthetic performance of seedlings from three oak species displaying different sensitivities (Quercus robur, Q. petraea and Q. rubra). Ann Sci For 54:409–429. doi:https://doi.org/10.1051/forest:19970501
Acknowledgments
We are grateful to the anonymous reviewers of the manuscript for their helpful comments.
Funding
This work was supported by the University of Franche-Comté and the regional council of Franche-Comté.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Erwin Dreyer
Contribution of the co-authors
Fabienne Tatin-Froux and Julien Parelle contributed to the entire study, and Nicolas Capelli contributed to writing the manuscript
Rights and permissions
About this article
Cite this article
Tatin-Froux, F., Capelli, N. & Parelle, J. Cause–effect relationship among morphological adaptations, growth, and gas exchange response of pedunculate oak seedlings to waterlogging. Annals of Forest Science 71, 363–369 (2014). https://doi.org/10.1007/s13595-013-0340-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13595-013-0340-6