New Forests

pp 1–20 | Cite as

Effect of combined stress (salinity + hypoxia) and auxin rooting hormone addition on morphology and growth traits in six Salix spp. clones

  • A. S. Quiñones MartorelloEmail author
  • M. E. Fernández
  • M. G. Monterubbianesi
  • M. N. Colabelli
  • P. Laclau
  • J. E. Gyenge


Willows plantations development could be an alternative for hydro-halomorphic soils but it is limited by combined stress salinity + hypoxia (main stressor under waterlogging conditions). We studied the effects of saline stress, alone or interacting with hypoxia, on growth, morphology and rooting process of six willows clones, assessing also whether rooting hormone (H, Indol Butyric Acid) contributes enhancing rooting under combined stress. Three hybrids of Salix matsudana × Salix alba (Sm×Sa), two of Salix babylonica × Salix alba (Sb×Sa) and a Salix nigra (Sn4) clone were evaluated in hydroponics. Ten treatments were generated combining salinity [moderate (MS): 5 dS/m, and high (HS): 10 dS/m]; hypoxia (with or without artificial aeration, HypO), and presence or absence of H. After 120 days, shoot and root biomass, root number and length, and hypertrophied lenticel number were evaluated. Contrary to what was expected, Sm×Sa and Sb×Sa hybrids showed no adverse additive effects of combined stress compared with saline stress; whereas in Sn4, S + HypO favored root biomass production increasing number and elongation of roots. Salinity was the main limiting factor for root production, being only MS conditions compatible with rooting, although limited. There was no common response in relation to H addition. In Sn4, H potentiated the effects of MS + HypO on root biomass, increasing number of roots. However, it had no positive effect on biomass production in the remaining hybrids, producing a higher root number but shorter in length. More effort is needed to understand the physiological mechanisms behind the response to combined stress in willows.


Willow Cuttings Indol butyric acid Hypertrophied lenticels Shoot and root biomass 



This work is part of A.Q.M doctoral studies supported by a CONICET fellowship, Argentina. The study was funded by Grants 300511-UCAR-MAGyP and PNFOR110473-INTA, Argentina.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11056_2019_9719_MOESM1_ESM.docx (1.4 mb)
Online Resource 1 Electrical Conductivity (EC) and pH measured in water of hydroponic systems during 120 days of treatment under combined stress and saline stress, applied to cuttings of six clones of Salix spp. Water samples were taken every 20 days to measure EC and pH. Treatments were Control, MS (moderate salinity, NaCl 5 dS/m), MS + HypO (moderate salinity + hypoxia); HS (high salinity, NaCl 10 dS/m) and HS + HypO (high salinity + hypoxia). The values correspond to the mean ± SE of three independent replicates. In the same treatment, means with a lowercase letter in common indicate no significant difference between measurement dates during the treatment (Tuckey test, P > 0.05). Means with a capital letter in common indicate no significant difference between treatments in the same date (Tuckey test, P > 0.05). (DOCX 1436 kb)
11056_2019_9719_MOESM2_ESM.docx (5.3 mb)
Online resource 2 Number of hypertrophied lenticels in six clones of Salix spp. under saline against combined stress. After 120 days of treatment the number of hypertrophied lenticels was evaluated in the total long cuttings of six clones of Salix exposed to the following treatments: Control, moderate salinity, NaCl 5 dS/m (MS), moderate salinity + hypoxia (MS + HypO), high salinity, NaCl 10 dS/m (HS) and high salinity + hypoxia (HS + HypO) (upper panel) and in three hybrids of Salix alba × Salix matsudana (‘524-50’, ‘NZ 26992’ and ‘Barrett 13-44 INTA’); two hybrids of Salix babylonica × Salix alba (‘Ragonese INTA 131-27’ and ‘Ragonese 131-25 INTA’) and Salix nigra‘Alonzo 4 INTA’ clone (lower panel). Mean ± SE with a lowercase letter in common indicate no significant differences between treatments considering all the clones together (upper panel) or between clones considering all the treatments together (lower panel) (LSD Fisher test P > 0.05). (DOCX 5477 kb)
11056_2019_9719_MOESM3_ESM.docx (3.5 mb)
Online resource 3 Shoot and root biomass production (gr per plant) in six Salix spp. clones exposed to combined stress versus saline stress alone. Mean ± SE with a lowercase letter in common between shoot biomass bars indicate no significant differences between clones (LSD Fisher test, P > 0.05). Mean ± SE with capital letter in common between root biomass bars indicate no significant differences between clones (LSD Fisher test, P > 0.05). The treatments without IBA addition were: Control, Moderate salinity (NaCl 5 dS/m), moderate salinity + hypoxia, high salinity (NaCl, 10 dS/m) and high salinity + hypoxia (HS + HypO). (DOCX 3540 kb)


  1. Allen JA, Pezeshki RS, Chambers JL (1996) Interaction of flooding and salinity stress on baldcypress (Taxodium distichum). Tree Physiol 16:307–313CrossRefGoogle Scholar
  2. Amlin NA, Rood SB (2001) Inundation tolerances of riparian willows and cottonwoods. JAWRA 37(6):1709–1720. Google Scholar
  3. Bailey-Serres J, Fukao T, Gibbs DJ et al (2012) Making sense of low oxygen sensing. Trends Plant Sci 3:129–138. CrossRefGoogle Scholar
  4. Barrett-Lennard EG (1986) Effects of waterlogging on the growth and NaCl uptake by vascular plants under saline conditions. Reclam Reveg Res 5:245–261Google Scholar
  5. Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant Soil 253:35–54CrossRefGoogle Scholar
  6. Barrett-Lennard EG, Shabala SN (2013) The waterlogging/salinity interaction in higher plants revisited focusing on the hypoxia-induced disturbance to K+ homeostasis. Funct Plant Biol 40(9):872–882CrossRefGoogle Scholar
  7. Beynon-Davies R, Sharp R (2013) Ethylene-auxin interactions during adventitious rooting in two populus hybrids of different rooting potential. In: Van Huylenbroeck J, Van Labeke MC, Van Laere K (eds) ISHS acta horticulturae II international symposium on woody ornamentals of the temperate zone, II symposium on woody perennials of the temperate zone, Ghent, Belgium, vol 990, pp 443–449Google Scholar
  8. Carter JL, Colmer TD, Veneklaas EJ (2006) Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes. New Phytol 169:123–134CrossRefGoogle Scholar
  9. Cerrillo T, Rodriguez ME, Achinelli F et al (2013) Do greenhouse experiments predict willow responses to long term flooding events in the field? Bosque 34(1):71–79CrossRefGoogle Scholar
  10. Chauhan AS, Naithani S, Balodi K et al (2015) Effects of plant growth hormones on Populus deltoides Bartram ex Marshall. An important species having potential in Agro-forestry. JSDC 2(2):344–349Google Scholar
  11. Da Costa CT, De Almeida MR, Ruedell CM et al (2013) When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 4:133–140CrossRefGoogle Scholar
  12. Fageria GD, Carvalho AB, Santos EP et al (2011) Chemistry of lowland rice soils and nutrient availability. Commun Soil Sci Plant Anal 42:1913–1933CrossRefGoogle Scholar
  13. Glenn E, Tanner R, Méndez S et al (1998) Growth rates, salt tolerance and water use characteristics of native and invasive riparian plants from the delta of the Colorado River, Mexico. J Arid Environ 40:281–294CrossRefGoogle Scholar
  14. Hangs RD, Schoenau JJ, Van Rees KCJ, Steppuhn H (2011) Examining the salt tolerance of willow (Salix sp.) bioenergy species for use on salt-affected agricultural lands. Can J Plant Sci 91:509–517CrossRefGoogle Scholar
  15. Hjelm K, Mc Carthy R, Rytter L (2018) Establishment strategies for poplars, including mulch and plant types, on agricultural land in Sweden. New For 49:737. CrossRefGoogle Scholar
  16. Isla R, Guillén M, Aragüés R (2014) Response of five tree species to salinity and waterlogging: shoot and root biomass and relationships with leaf and root ion concentrations. AgroforSyst 88:461–477Google Scholar
  17. Jackson MB, Attwood PA (1996) Roots of willow (Salix viminalis L.) show marked tolerance to oxygen shortage in flooded soils and in solution culture. Plant Soil 187:37. CrossRefGoogle Scholar
  18. Jarrell WM, Virginia RA (1990) Response of mesquite to nitrate and salinity in a simulated phreatic environment: water use, dry matter and mineral nutrient accumulation. Plant Soil 125(2):185–196CrossRefGoogle Scholar
  19. Kozlowski TT, Kramer PJ, Pallardy SG (1991) The physiological ecology of woody plants. Academic Press, San DiegoGoogle Scholar
  20. Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol Monogr 1:1–28Google Scholar
  21. Kozlowski TT, Pallardy SG (1997) Physiology of woody plants, 2nd edn. Academic Press, San Diego, p 411Google Scholar
  22. Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259Google Scholar
  23. Laclau P, Gyenge J, Fernández ME et al (2014) Supervivencia inicial de clones de sauce en suelos hidrohalomórficos de Depresión del Salado. IV Congreso Internacional de Salicáceas en Argentina Sauces y Álamos para el desarrollo regional, La Plata, Buenos Aires, ArgentinaGoogle Scholar
  24. Liu M, Qiao G, Jiang J et al (2014) Identification and expression analysis of salt-responsive genes using a comparative microarray approach in Salix matsudana. MolBiol Rep 41:6555–6568. Google Scholar
  25. Marcar NE (1993) Waterlogging modifies growth, water use and ion concentrations in seedlings of salt-treated E. camaldulensis, E. tereticornis, E. robustaand E. globulus. Funct Plant Biol 20:1–13CrossRefGoogle Scholar
  26. Markus-Michalczyk H, Hanelt D, Jensen K (2016) Effects of tidal flooding on juvenile willows. Estuaries Coasts 39:397–405. CrossRefGoogle Scholar
  27. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Physiol 59:651–681Google Scholar
  28. Noble CL, Rogers ME (1994) Response of temperate forest legumes to waterlogging and salinity. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker Inc., New York, pp 473–496Google Scholar
  29. Pacurar DI, Perrone I, Bellini C (2014) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant 151:83–96CrossRefGoogle Scholar
  30. Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286CrossRefGoogle Scholar
  31. Pezeshki SR, Anderson PH, Shields FD (1998) Effects of soil moisture regimes on growth and survival of black willow (Salix nigra) posts (cuttings). Wetlands 18:460–470CrossRefGoogle Scholar
  32. Pierce S, Koontz M, Pezeshki SR, Kröger R (2013) Response of Salix nigra [Marsh.] cuttings to horizontal asymmetry in soil saturation. Environ Exp Bot 87:137–147CrossRefGoogle Scholar
  33. Plante PM, Rivest D, Vézina A, Vanasse A (2014) Root distribution of different mature tree species growing on contrasting textured soils in temperate windbreaks. Plant Soil. Google Scholar
  34. Quiñones Martorello AS, Gyenge JE, Fernández ME (2017) Morpho-physiological response to vertically heterogeneous soil salinity of two glycophyte woody taxa, Salix matsudana × S. alba and Eucalyptus camaldulensis Dehnh. Plant Soil 12:3. Google Scholar
  35. Rodríguez ME, Doffo GN, Cerrillo T, Luquez VMC (2018) Acclimation of cuttings from different willow genotypes to flooding depth level. New For 49:415–427. CrossRefGoogle Scholar
  36. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 20 Nov 2016
  37. Rossi P (1999) Length of cuttings in establishment and production of short rotation plantations of Salix “Aquatica”. New For 18:161–177CrossRefGoogle Scholar
  38. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617. CrossRefGoogle Scholar
  39. Van Der Moezel PG, Pearce-Pinto GVN, Bell DT (1991) Screening for salt and waterlogging tolerance in Eucalyptus and Melaleuca species. For Ecol Manag 40:27–37CrossRefGoogle Scholar
  40. Vidoz ML, Loreti E, Mensuali A et al (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562CrossRefGoogle Scholar
  41. Wan X, Tandy S, Hockmann K, Schulin R (2013) Changes in Sb speciation with waterlogging of shooting range soils and impacts on plant uptake. Environ Pollut 172:53–60CrossRefGoogle Scholar
  42. Wang R, Dai S, Tang S et al (2012) Growth, gas exchange, root morphology and cadmium uptake responses of poplars and willows grown on cadmium-contaminated soil to elevated CO2. Environ Earth Sci 67(1):1–13CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.CONICET, Consejo Nacional de Investigaciones Científicas y TécnicasCABAArgentina
  2. 2.INTA EEA Balcarce- AETandilTandilArgentina
  3. 3.Facultad AgronomíaUNMDPBalcarceArgentina
  4. 4.INTA EEA Bariloche- AESan Martín de los AndesSan Martín de los AndesArgentina

Personalised recommendations