Abstract
It was suggested that Na+ ions could play a vital role in the growth of xero-halophyte Atriplex halimus. This study aims at investigating the impact of Na+ ions on the response of droughted A. halimus seedlings to the recovery in the natural habitat. The time-course regulation of recovery-responsive genes and the changes in physiological attributes during the recovery were examined in the absence (RW) or presence of 300 mM NaCl (RS). After 30 min and up to the end of the experiment, photosynthetic rate (A), stomatal conductance (gs) and leaf fresh and dry weights (FW) were enhanced by RW. Meanwhile, there was a sudden decline in (A) and (gs) rates after 30 min followed by a recovery in both rates after 3 h of RS. In response to RS, the change in carbon and nitrogen balance may act as a signal to regulate (A) and (gs) rates, in an attempt to control the upload of Na+ ions via transpiration. After 30 min or 3 h of the RW or RS onset, respectively, 1) the increase in 9-cis epoxycarotenoid dioxygenase (NCEDs) and abscisic acid (ABA) levels could stimulate the recovery-responsive genes rather than controlling (gs) and 2) the induction of ABA-dependent/independent transcription factors and recovery/salt-inducible genes could suggest their effective contributions to the recovery adaptation. After 5 d of the recovery onset, RS lowered FW by 82% whereas RW increased FW by 110%. Na+ ions could not enhance the performance of A. halimus seedlings during the recovery, perhaps, due to the non-constitutive expression of salt-responsive genes.
Similar content being viewed by others
Abbreviations
- A :
-
Photosynthetic rate
- ABI3, 5 :
-
Abscisic acid insensitive 3, 5
- C i :
-
Leaf internal CO2 concentration
- CMO :
-
Choline monooxygenase
- DREB1, 2, E :
-
Dehydration Responsive Element Binding 1, 2, E
- E :
-
Transpiration rate
- g s :
-
Stomatal conductance
- NHX1 :
-
Vacuolar sodium/hydrogen antiporter
- SOS1 :
-
Salt overly sensitive (Plasma membrane sodium/ hydrogen antiporter)
- RW:
-
Recovery with water
- RS:
-
Recovery with water supplemented with 300 mM NaCl
- RWC:
-
Relative water content
- WUE :
-
Water use efficiency
- PEPC:
-
Phosphoenol pyruvate carboxylase
- TF:
-
Transcription factor
- EC:
-
Electric conductivity
- FC:
-
Field capacity
- TSS:
-
Total soluble sugar
References
Abbad A, Benchaabane A (2004) The phonological study of Atriplex halimus L. Afri J Ecol 42:69–73
Apse MP, Blumwald E (2002) Engineering salt tolerance. Cur Opin Biotech 13:146–150
Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239
Atif R, Shahid L, Waqas M, Ali B, Rashid M, Azeem F, Nawaz MA, Wani SH, Chung G (2019) Insights on calcium-dependent protein kinases (CPKs) signaling for abiotic stress tolerance in plants. Int J Mol Sci 20:5298
Auler PA, do Amaral MN, Rodrigues GS, Benitez LC, Maia LC, Souza GM, Braga EJB (2017) Molecular responses to recurrent drought in two contrasting rice genotypes. Planta 246:899–914
Bahrami-Rad S, Hajiboland R (2017) Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: comparison of root with foliar application. Ann Agric Sci 62(2):121–130
Bajji M, Kinet JM, Lutts S (2002) Osmotic and ionic effects of NaCl on germination, early seedling growth, and ion content of Atriplex halimus (Chenopodiaceae). Can J Bot 80:297–304
Bedi S, Sengupta S, Ray A, Chaudhuri RN (2016) ABI3 mediates dehydration stress recovery response in Arabidopsis thaliana by regulating expression of downstream genes. Plant Sci 250:125–140
Brignone NF, Denham SS, Pozner R (2016) Synopsis of the genus Atriplex (Amaranthaceae, Chenopodioideae) for South America. Aust Syst Bot 29:324–357. https://doi.org/10.1071/SB16026
Chater CCC, Oliver J, Casson S, Gray JE (2014) Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development. New Phytol 202:376–391
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng X, Xiong L (2008) Integration of light and abscisic acid signalling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500
Engineer C, Hashimoto-Sugimoto M, Negi J, Nordstrom MI, Azoulay-Shemer T, Rappel WJ, Iba K, Schroeder J (2016) CO2 sensing and CO2 regulation of stomatal conductance: advances and open questions. Trends Plant Sci 21:16–30
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signalling in seeds and seedlings. Plant Cell 14:S15–S45
Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127:343–352
Flexas J, Barón M, Bota J, Ducruet JM, Gallé A, Galmés J, Jiménez M, Pou A, Ribas-Carbó M, Sajnani C, Tomàs M, Medrano H (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri × V. rupestris). J Exp Bot 60:2361–2377
Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential oh halophytes. Cri Rev Plant Sci 18:227–255
Hansen EH, Munns DN (1988) Effect of CaSO4 and NaCl on mineral content of Leucaena leucocephala. Plant Soil 7:101–105
Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271
Hayashi H, Murata N (1998) Genetically engineered enhancement of salt tolerance in higher plants. In: Satoh K, Murata N (eds) Stress responses of photosynthetic organisms. Elsevier, Amsterdam, pp 133–148
Henson IE, Mahalakshmi V, Alagarswamy G, Bidinger FR (1984) Leaf abscisic acid content and recovery from water stress in pearl millet (Pennisetum americanum [L.] Leeke). J Exp Bot 35:99–109
Hsiao TC, Läuchli A (1986) A role of potassium in plant water relations. In: Tinker B, Läuchli A (eds) Advances in plant nutrition, 2nd edn. Praeger Scientific, New York, pp 281–312
Hunte C, Screpanti E, Venturi M, Rimon A, Padan E, Michel H (2005) Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435:1197–1202
Joffre R, Rambal S, Damesin C (1999) Functional attributes in mediterranean-type ecosystems. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker Inc., New York, pp 347–380
Kaiser WM (1987) Effects of water deficit on photosynthetic capacity. Physiol Plant 71:142–149
Kandel ER, Dudai Y, Mayford MR (2014) The molecular and systems biology of memory. Cell 157:163–186
Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophile. Plant Cell Environ 29:1220–1234
Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:18816–18821
Khedr AA, Serag MS, Nemat-Alla MM, Abo-Elnaga AZ, Nada RM, Quick WP, Abogadallah GM (2011) A DREB gene from the xero-halophyte Atriplex halimus is induced by osmotic but not ionic stress and shows distinct differences from glycophytic homologues. Plant Cell Tis Org Cult 106:191–206
Kromdijk J, Schepers HE, Albanito F, Fitton N, Carroll F, Jones MB, Finnan J, Lanigan GJ, Griffiths H (2008) Bundle sheath leakiness and light limitation during C4 leaf and canopy CO2 uptake. Plant Physiol 148:2144–2155
Laemmlli EK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nat 227:680–685
Lee SC, Lim CW, Lan W, He K, Luan S (2012) ABA signaling in guard cells entails a dynamic protein–protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol Plant 6:528–538
Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J 37:720–729
Martınez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot 56:2421–2431
McAdam SA, Brodribb TJ (2012) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24:1510–1521
McArthur ED, Sanderson SC (1984) Distribution, systematics, and evolution of Chenopodiaceae: an overview: In: Tiedemann AR, McArthur ED, Stutz HC, Stevens R, Johnson KL, comps. Proceedings, Symposium on the Biology of Atriplex and related chenopods; 1983 May 4–6; Provo, UT. Gen.Tech. Rep. INT-172. Ogden, UT: USDA Forest Service, Inter For Range Exp Stat 14–23.
Mehrotram R, Bhalothia P, Bansal P, Basantanid MK, Bhartie V, Mehrotra S (2014) Abscisic acid and abiotic stress tolerance–different tiers of regulation. J Plant Physiol 171:486–496
Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ Exp Bot 53:205–214
Murata S, Kobayashi M, Matoh T, Sekiya J (1992) Sodium stimulates regeneration of phosphoenolpyruvate in mesophyll chloroplasts of chloroplasts of Amaranthus tricolor. Plant Cell Physiol 33:1247–1250
Nada RM, Abogadallah GM (2014) Aquaporins are major determinants of water use efficiency of rice plants in the field. Plant Sci 227:165–180
Nada RM, Abogadallah GM (2015) Developmental acquisition of salt tolerance in the halophyte Atriplex halimus L. is related to differential regulation of salt inducible genes. Plant Growth Regul 75:165–178
Nada RM, Khedr AA, Serag MS, El-Qashlan NR, Abogadallah GM (2018) Maturation of Atriplex halimus L. leaves involves changes in the molecular regulation of stomatal conductance under high evaporative demand and high but not low soil water content. Planta 248:795–812
Ohnishi J, Flügge U, Heldt HW, Kanai R (1990) Involvement of Na+ in active uptake of pyruvate in mesophyll chloroplasts of some C4 plants: Na+/pyruvate cotransport. Plant Physiol 94:950–959
Okamoto M, Peterson FC, Defries A, Park SY, Endo A, Nambara E, Volkman BF, Cutler SR (2013) Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. Proc Natl Acad Sci USA 110:12132–12137
Orrego F, Ortiz-Calderónc C, Luttsd S, Ginocchioa R (2020) Growth and physiological effects of single and combined Cu, NaCl, and water stresses on Atriplex atacamensis and A. halimus. Environ Exp Bot 169:103919
Osmond CB Björkman O, Anderson DJ (1980) Physiological processes in plant ecology: towards a synthesis with Atriplex. Springer-Verlag, Berlin
Parcy F, Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J 11:693–702
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400
Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr.) Wats. Plant Physiol 59:795–799
Pego JV, Kortstee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416
Perez-Martin A, Michelazzo C, Torres-Ruiz JM, Flexas J, Fernández J, Sebastiani L, Diaz-Espejo A (2014) Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: correlation with gene expression of carbonic anhydrase and aquaporins. J Exp Bot 65:3143–3156
Pierce M, Raschke K (1981) Synthesis and metabolism of abscisic acid in detached leaves of Phuseolus vulguris after loss and recovery of turgor. Planta 153:156–165
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882
Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384
Sabovljevic´ M, Sabovljevic´ A (2007) Contribution to the coastal bryophytes of the Northern Mediterranean: are there halophytes among bryophytes? Physiol Bot 13:131–135
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Streb P, Shang W, Feierabend J, Bligny R (1998) Divergent strategies of photoprotection in high-mountain plants. Planta 207:313–324
Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432
Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Nat Sci Rep 5:12449
Tuteja N, Mahajan S (2007) Calcium signaling network in plants. Plant Signal Behav 2:79–85
Ungar IA (1978) Halophyte seed germination. Bot Rev 44:233–264
Wang W, Zhang H, Wei X, Yang L, Yang B, Zhang L, Li J, Jiang Y-Q (2018) Functional characterization of calcium-dependent protein kinase (CPK) 2 gene from oilseed rape (Brassica napus L.) in regulating reactive oxygen species signaling and cell death control. Gene 651:49–56
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Freidit FN, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217
Yao G, Li F, Nie Z, Bi M, Jiang H, Liu X, Wei Y, Fang X (2020) Ethylene, not ABA, is closely linked to the recovery of gas exchange after drought in four Caragana species. Plant Cell Environ 44(2):399–411
Yeo ER (1998) Molecular biology of salt tolerance in the context of whole plant physiology. J Exp Bot 49:915–929
Yue Y, Zhang M, Zhang J, Duan L, Li Z (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. J Plant Physiol 169:255–261
Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273
Author information
Authors and Affiliations
Contributions
RN and GA designed the research and contributed to fieldwork and data interpretation. AK designed the research and contributed to fieldwork and data interpretation. MS helped in fieldwork and contributed to interpretation. RN and NA performed the experiments, collected the data and also contributed to data analysis. NA did the molecular and biochemical analyses. RN designed and supervised the molecular and biochemical analyses, did some of the molecular analyses and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Handling Editor: Rhonda Peavy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nada, R.M., Khedr, A.H.A., Serag, M.S. et al. Molecular and Physiological Responses of Naturally Grown Atriplex halimus L. to Drought-Stress Recovery in the Absence or Presence of Na+ Ions Under Natural Conditions. J Plant Growth Regul 41, 1578–1593 (2022). https://doi.org/10.1007/s00344-021-10398-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10398-z