Environmental factors constraining adventitious root formation during flooding of Solanum dulcamara
Qian Zhang A , Heidrun Huber A , Jannah W. T. Boerakker A , Daniek Bosch A , Hans de Kroon A and Eric J. W. Visser A BA Department of Experimental Plant Ecology, Institute for Water and Wetland Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands.
B Corresponding author. Email: eric.visser@science.ru.nl
Functional Plant Biology 44(9) 858-866 https://doi.org/10.1071/FP16357
Submitted: 14 October 2016 Accepted: 31 January 2017 Published: 29 March 2017
Abstract
Flooding is a compound stress, imposing strong limitations on plant development. The expression of adaptive traits that alleviate flooding stress may be constrained if floodwater levels are too deep. For instance, adventitious root outgrowth is typically less profound in completely submerged plants than in partially submerged plants, suggesting additional constraints in full submergence. As both oxygen and carbohydrates are typically limited resources under submergence, we tested the effects of oxygen concentration in the floodwater and carbohydrate status of the plants on flooding-induced adventitious root formation in Solanum dulcamara L. Partially submerged plants continued to form adventitious roots in low-oxygen floodwater, whereas completely submerged plants developed hardly any roots, even in floodwater with twice the ambient oxygen concentration. This suggests that contact with the atmosphere, enabling internal aeration, is much more important to optimal adventitious root formation than floodwater oxygen concentrations. If plants were depleted of carbohydrates before flooding, adventitious root formation in partial submergence was poor, unless high light was provided. Thus, either stored or newly produced carbohydrates can fuel adventitious root formation. These results imply that the impact of an environmental stress factor like flooding on plant performance may strongly depend on the interplay with other environmental factors.
Additional keywords: carbohydrates, light, oxygen, shade, submergence, waterlogging.
References
Altman A, Wareing PF (1975) The effect of IAA on sugar accumulation and basipetal transport of 14C-labelled assimilates in relation to root formation in Phaseolus vulgaris cuttings. Physiologia Plantarum 33, 32–38.| The effect of IAA on sugar accumulation and basipetal transport of 14C-labelled assimilates in relation to root formation in Phaseolus vulgaris cuttings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhsFSgur8%3D&md5=2b26d324b900887085c0f780e9d81856CAS |
Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 236–332.
Armstrong W, Drew MC (2002) Root growth and metabolism under oxygen deficiency. In ‘Plant roots: the hidden half’. (3rd edn) (Eds Y Waisel, A Eshel, U Kafkafi) pp. 729–761. (Marcel Dekker, New York)
Armstrong W, Webb T (1985) A critical oxygen pressure for root extension in rice. Journal of Experimental Botany 36, 1573–1582.
| A critical oxygen pressure for root extension in rice.Crossref | GoogleScholarGoogle Scholar |
Ayi Q, Zeng B, Liu J, Li S, van Bodegom PM, Cornelissen JHC (2016) Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants. Annals of Botany 118, 675–683.
| Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants.Crossref | GoogleScholarGoogle Scholar |
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
| Flooding stress: acclimations and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsLc%3D&md5=d90a6c2ec0e60f70cf1ac88123e7f803CAS |
Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698–1709.
| Waterproofing crops: effective flooding survival strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt73E&md5=837dcf1844c946482fb56732ab57bcb5CAS |
Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology 116, 1515–1526.
| Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFyqt7o%3D&md5=b3efd64babef274a6af8e80e8661288aCAS |
Chen X, Pierik R, Peeters AJM, Poorter H, Visser EJW, Huber H, de Kroon H, Voesenek LACJ (2010) Endogenous abscisic acid as a key switch for natural variation in flooding-induced shoot elongation. Plant Physiology 154, 969–977.
| Endogenous abscisic acid as a key switch for natural variation in flooding-induced shoot elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCkt7bN&md5=05e04c10708e5ebffc5fa837c5e2013eCAS |
Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
| Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurnE&md5=99126213578359bcfb5543995a40fdd2CAS |
Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
| Flooding tolerance: suites of plant traits in variable environments.Crossref | GoogleScholarGoogle Scholar |
Colmer TD, Cox MCH, Voesenek LACJ (2006) Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations. New Phytologist 170, 767–778.
| Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmslSisL0%3D&md5=c46ca69c1fb754d5f8abf28def0a2f81CAS |
Corrêa LR, Paim DC, Schwambach J, Fett-Neto AG (2005) Carbohydrates as regulatory factors on the rooting of Eucalyptus saligna Smith and Eucalyptus globulus Labill. Plant Growth Regulation 45, 63–73.
| Carbohydrates as regulatory factors on the rooting of Eucalyptus saligna Smith and Eucalyptus globulus Labill.Crossref | GoogleScholarGoogle Scholar |
Das KK, Sarkar RK, Ismail AM (2005) Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice. Plant Science 168, 131–136.
| Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsFSltbk%3D&md5=6b55fe4cc93e8d72c8a99d7825644518CAS |
Dawood T, Rieu I, Wolters-Arts M, Derksen EB, Mariani C, Visser EJW (2014) Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara. AoB Plants 6, plt058
| Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara.Crossref | GoogleScholarGoogle Scholar |
Drew MC, Sisworo EJ (1979) The development of waterlogging damage in young barley plants in relation to plant nutrient status and changes in soil properties. New Phytologist 82, 301–314.
| The development of waterlogging damage in young barley plants in relation to plant nutrient status and changes in soil properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltlWmtbs%3D&md5=496db780eeea9580f95668775b80874fCAS |
Druege U, Zerche S, Kadner R (2004) Nitrogen- and storage-affected carbohydrate partitioning in high-light-adapted Pelargonium cuttings in relation to survival and adventitious root formation under low light. Annals of Botany 94, 831–842.
| Nitrogen- and storage-affected carbohydrate partitioning in high-light-adapted Pelargonium cuttings in relation to survival and adventitious root formation under low light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Wmuw%3D%3D&md5=616e1b3de2d911ea1dc72c3fa656a389CAS |
Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell 18, 2021–2034.
| A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1KjtLg%3D&md5=9b53635a8b8be777dfcc334047b3b46aCAS |
Groeneveld HW, Voesenek LACJ (2003) Submergence-induced petiole elongation in Rumex palustris is controlled by developmental stage and storage compounds. Plant and Soil 253, 115–123.
| Submergence-induced petiole elongation in Rumex palustris is controlled by developmental stage and storage compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemtr8%3D&md5=31aed460a415f48ef5987f98aa1a8f1fCAS |
Guglielminetti L, Yamaguchi J, Perata P, Alpi A (1995) Amylolytic activities in cereal seeds under aerobic and anaerobic conditions. Plant Physiology 109, 1069–1076.
| Amylolytic activities in cereal seeds under aerobic and anaerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsVOrtrs%3D&md5=a4010d1299aec2a45f1535cac983df7bCAS |
Herzog M, Pedersen O (2014) Partial versus complete submergence: snorkelling aids root aeration in Rumex palustris but not in R. acetosa. Plant, Cell & Environment 37, 2381–2390.
Huber H, Chen X, Hendriks M, Keijsers D, Voesenek LACJ, Pierik R, Poorter H, de Kroon H, Visser EJW (2012) Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage. New Phytologist 194, 572–582.
| Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage.Crossref | GoogleScholarGoogle Scholar |
Laan P, Berrevoets MJ, Lythe S, Armstrong W, Blom CWPM (1989) Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species. Journal of Ecology 77, 693–703.
| Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species.Crossref | GoogleScholarGoogle Scholar |
Laan P, Tosserams M, Blom CWPM, Veen BW (1990) Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions. Plant and Soil 122, 39–46.
| Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions.Crossref | GoogleScholarGoogle Scholar |
Lorbiecke R, Sauter M (1999) Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiology 119, 21–30.
| Adventitious root growth and cell-cycle induction in deepwater rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Gmtg%3D%3D&md5=ff70f019fefd6aa3bd40a5d15ed8db99CAS |
Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96, 581–589.
| Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitLnE&md5=dbfa0f2525706626807ea3ae67ecb8dbCAS |
Mommer L, Pons TL, Visser EJW (2005) Photosynthetic consequences of phenotypic plasticity in response to submergence: Rumex palustris as a case study. Journal of Experimental Botany 57, 283–290.
| Photosynthetic consequences of phenotypic plasticity in response to submergence: Rumex palustris as a case study.Crossref | GoogleScholarGoogle Scholar |
Nielsen SL (1993) A comparison of aerial and submerged photosynthesis in some Danish amphibious plants. Aquatic Botany 45, 27–40.
| A comparison of aerial and submerged photosynthesis in some Danish amphibious plants.Crossref | GoogleScholarGoogle Scholar |
Perata P, Guglielminetti L, Alpi A (1997) Mobilization of endosperm reserves in cereal seeds under anoxia. Annals of Botany 79, 49–56.
| Mobilization of endosperm reserves in cereal seeds under anoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlWrs7s%3D&md5=a6baa80317d6e1ae1b230ccee5bea50aCAS |
R Development Core Team (2014) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at http://www.R-project.org/. [Verified 9 February 2017]
Rich SM, Ludwig M, Colmer TD (2012) Aquatic adventitious root development in partially and completely submerged wetland plants Cotula coronopifolia and Meionectes brownii. Annals of Botany 110, 405–414.
| Aquatic adventitious root development in partially and completely submerged wetland plants Cotula coronopifolia and Meionectes brownii.Crossref | GoogleScholarGoogle Scholar |
Sauter M (2013) Root responses to flooding. Current Opinion in Plant Biology 16, 282–286.
| Root responses to flooding.Crossref | GoogleScholarGoogle Scholar |
Soffer H, Burger DW (1988) Effects of dissolved oxygen concentrations in aero-hydroponics on the formation and growth of adventitious roots. Journal of the American Society for Horticultural Science 113, 218–221.
Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiology 170, 603–617.
| The physiology of adventitious roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1WjsbfK&md5=400b018ef2c268d624cf6a2edd567155CAS |
Striker GG, Manzur ME, Grimoldi AA (2011) Increasing defoliation frequency constrains regrowth of the forage legume Lotus tenuis under flooding. The role of crown reserves. Plant and Soil 343, 261–272.
| Increasing defoliation frequency constrains regrowth of the forage legume Lotus tenuis under flooding. The role of crown reserves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFSksL8%3D&md5=38e73402e93b76e569b2adede9b4be36CAS |
van der Sman AJM, Blom CWPM, Barendse GWM (1993) Flooding resistance and shoot elongation in relation to developmental stage and environmental conditions in Rumex maritimus L. and Rumex palustris Sm. New Phytologist 125, 73–84.
| Flooding resistance and shoot elongation in relation to developmental stage and environmental conditions in Rumex maritimus L. and Rumex palustris Sm.Crossref | GoogleScholarGoogle Scholar |
Visser EJW, Blom CWPM, Voesenek LACJ (1996) Flooding-induced adventitious rooting in Rumex: morphology and development in an ecological perspective. Acta Botanica Neerlandica 45, 17–28.
| Flooding-induced adventitious rooting in Rumex: morphology and development in an ecological perspective.Crossref | GoogleScholarGoogle Scholar |
Visser EJW, Nabben RHM, Blom CWPM, Voesenek LACJ (1997) Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations. Plant, Cell & Environment 20, 647–653.
| Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFamu78%3D&md5=72aa60efa85cd1afe2295be5a585b16bCAS |
Voesenek LACJ, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytologist 206, 57–73.
| Flood adaptive traits and processes: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtF2qs78%3D&md5=76423899a4d43100a45ac77132b6b06eCAS |
Voesenek LACJ, Banga M, Thier RH, Mudde CM, Harren FJM, Barendse GWM, Blom CWPM (1993) Submergence-induced ethylene synthesis, entrapment, and growth in two plant species with contrasting flooding resistances. Plant Physiology 103, 783–791.
| Submergence-induced ethylene synthesis, entrapment, and growth in two plant species with contrasting flooding resistances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXntlKqtQ%3D%3D&md5=5ef935f038e91b2799088cc954fac558CAS |
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213–226.
| How plants cope with complete submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFamtLw%3D&md5=d00fab0c7667de204b8722ff9e4242a4CAS |
Wiengweera A, Greenway H (2004) Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation. Journal of Experimental Botany 55, 2121–2129.
| Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVyit74%3D&md5=c3e1798d4467f7ca026a9f342521437bCAS |
Winkel A, Pedersen O, Ella E, Ismail AM, Colmer TD (2014) Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. Journal of Experimental Botany 65, 3225–3233.
| Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Wqu73P&md5=e206445114c1fbb62640e164bbd59414CAS |
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514.
| The estimation of carbohydrates in plant extracts by anthrone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXlvFOmtw%3D%3D&md5=0d802fd9c4c92aee18823d48d3afefb9CAS |
Zhang Q, Visser EJW, de Kroon H, Huber H (2015) Life cycle stage and water depth affect flooding-induced adventitious root formation in the terrestrial species Solanum dulcamara. Annals of Botany 116, 279–290.
| Life cycle stage and water depth affect flooding-induced adventitious root formation in the terrestrial species Solanum dulcamara.Crossref | GoogleScholarGoogle Scholar |