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Contribution of structural and functional adaptations of hyper-accumulator Suaeda vera Forssk. ex J.F. Gmel. for adaptability across salinity gradients in hot desert

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Abstract

The role of ionic excretions and hyper-accumulation of salts through alterations of structural and functional traits in five populations of Suaeda vera Forssk. ex J.F. Gmel., a halophytic salt-indicator species of saline environments, was explored. Differently adapted populations of S. vera exhibited specific structural and functional responses for the survival in hyper-saline conditions. Better growth in population from moderately saline habitat (25–30 dS m−1) was linked to high shoot and root K+ and increased ion selectivity (K+/Na+ and Ca2+/Na+). Increased excretion of Na+ and Cl− with increasing salinity level was a critical mechanism in maintaining ionic balance. Drastic differences were observed for anatomical characteristics in populations inhabiting differentially salt-affected lands. The plants from highly saline sites were characterized by narrow metaxylem vessels, low proportion of cortical parenchyma, and reduced phloem area leading to stunted growth. Contrariwise, root area significantly increased due to high proportion of sclerified xylem tissue, which was associated with easier conduction of solutes and protection of roots from collapsing. Root sclerification particularly at the highest salinity regime was a key factor in the survival of this species in salt-affected compact soils. Leaf anatomical characteristics showed reduction with increasing salinity, but the leaf thickness responded otherwise. This contributed to increased leaf succulence because of high proportion of storage parenchyma in populations colonizing hyper-saline habitats. It was concluded that moderate salinity conditions were more suitable for the growth of S. vera, though some populations of this species were able to tolerate much higher salinity levels.

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Data availability

The data has been submitted to the digital repository of the Department of Botany, University of Agriculture, Faisalabad and can be obtained by request to the corresponding author.

Abbreviations

BD:

Bailahwala Dahar

Ca:

Soil Ca2+

Cl:

Soil Cl−

Com:

Community

DF:

Derawar Fort

DI:

Shannon’s diversity index

Dsb:

Disturbances

ECa:

Excreted Ca2+

EC:

Electrical conductivity of soil extract

ECl:

Excreted Cl−

EK:

Excreted K+

EMg:

Extracted Mg2+

ENa:

Excreted Na+

ENO:

Extracted NO3−

EPO:

Extracted PO43−

IV:

Importance value

K:

Soil K+

Lar:

Leaf area

LBA:

Leaf abaxial epidermal cell area

LCA:

Leaf cortical cell area

LCT:

Leaf cortical region thickness

LDA:

Leaf adaxial epidermal cell area

LMT:

Leaf midrib thickness

LPA:

Leaf phloem area

LPS:

Leaf palisade cell area

LS:

Ladam Sir

LSP:

Leaf spongy cell area

LXA:

Leaf metaxylem area

MC:

Moisture content

Mg:

Soil Mg2+

MLGP:

Moderately livestock grazing pressure

Na:

Soil Na+

NO:

Soil NO3−

OM:

Organic matter

OP:

Osmotic potential

Phn:

Phenology

pH:

Soil pH

PO:

Soil PO43−

PrC:

Proportion of cortical parenchyma

PrP:

Proporion of storage parenchyma

PS:

Pati Sir

RAr:

Root cross-sectional area

RCa:

Root Ca2+

RCA:

Root cortical cell area

RCl:

Root Cl−

RC:

Relative cover

RCa:Na:

Root Ca2+:Na+ ratio

RCT:

Root cortical region thickness

RD:

Relative density

RDW:

Root dry weight

RF:

Relative frequency

RFW:

Root fresh weight

RK:

Root K+

RK:Na:

Root K+:Na+ ratio

Rlg:

Root length

RMg:

Root Mg2+

RNa:

Root Na+

RPA:

Root phloem area

RPO:

Shoot PO43−

RVT:

Root vascular region area

RWC:

Roor water content

RXA:

Root metaxylem area

SAR:

Sodium adsorption ratio

SA:

Stem area

SBA:

Abaxial stomatal area

SBD:

Abaxial stomatal density

SCa:

Shoot Ca2+

SCA:

Stem cortical cell area

SCa:Na:

Shoot Ca2+:Na+ ratio

SCl:

Shoot Cl−

SCT:

Stem cortical region thickness

SDA:

Abaxial stomatal area

SDb:

Slightly disturbed

SDD:

Adaxial stomatal density

SDW:

Shoot dry weight

SEA:

Stem epidermal cell area

SFW:

Shoot fresh weight

SK:

Shoot K+

SK:Na:

Shoot K+:Na+ ratio

Slg:

Shoot length

SMg:

Shoot Mg2+

SNa:

Shoot Na+

SPA:

Stem phloem area

SPC:

Stem pith cell area

SPO:

Shoot PO43−

SP:

Saturation percentage

SPT:

Stem pith thickness

Suc:

Succulence

SWC:

Shoot water content

SXA:

Stem metaxylem area

TSS:

Total soluble salts

TT:

Trawaywala Toba

UDb:

Undisturbed

References

  • Albaho MS, Green JL (2000) Suaeda salsa, a desalinating companion plant for greenhouse tomato. HortScience 35:620–623

    Article  Google Scholar 

  • Al-maskri A, Hameed M, Ashraf M, Khan MM, Fatima S, Nawaz T, Batool R (2014) Structural features of some wheat (Triticum Spp.) landraces/cultivars under drought and salt stress. Arid Land Res Manage 28:355–370

    Article  CAS  Google Scholar 

  • Arshad M, Akbar G (2002) Benchmark of plant communities of Cholistan Desert. Pak J Biol Sci 5:1110–1113

    Article  Google Scholar 

  • Arshad M, Ashraf MY, Ahmad M, Zaman F (2007) Morpho-genetic variability potential of Cenchrus ciliaris L. from Cholistan Desert. Pakistan Pak J Bot 39:1481–1488

    Google Scholar 

  • Arshad M, Anwar-ul-Hussan AMY, Noureen S, Moazzam M (2008) Edaphic factors and distribution of vegetation in the Cholistan Desert, Pakistan. Pak J Bot 40:1923–1931

    Google Scholar 

  • Arshad M, Hussain I, Ashraf MY, Noureen S, Mukhtar M (2009) Study on agromorphological variation in germplasm of Lasiurus scindicus from Cholistan Desert, Pakistan. Pak J Bot 41:1331–1337

    Google Scholar 

  • Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–495

    Article  Google Scholar 

  • Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). www.canoco.com

  • Dehan K, Tall M (1978) Salt tolerance of the wild relatives of the cultivated tomato: responses of Solanum pennellii to high salinity. Irrigat Sci 1:71–76

    Article  Google Scholar 

  • Duan H, Ma Y, Liu R, Li Q, Yang Y, Song J (2018) Effect of combined waterlogging and salinity stresses on euhalophyte Suaeda glauca. Plant Physiol Biochem 127:231–237

    Article  CAS  Google Scholar 

  • El-Maboud MMA, Khalil RMA (2013) Ecophysiological and genetic studies on some species of the genus Suaeda Forssk ex Scop. in the Mediterranean Sea Coast. World Appl Sci J 27:811–825

    Google Scholar 

  • Fatima S, Hameed M, Naz N, Shah SMR, Naseer M, Ahmad MSA, Ashraf M, Ahmad F, Khalil S, Ahmad I (2021) Survival strategies in khavi grass [Cymbopogon jwarancusa (Jones) Schult.] colonizing hot hypersaline and arid environments. Water Air Soil Pollut 232:82

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  Google Scholar 

  • Freitag H, Hedge IC, Jaffri SMH (2001) Chenopodiaceae. Flora of Pakistan 204. Missouri Botanical Garden Press and the University of Karachi, Karachi, pp 1–218

  • Gadallah MAA, Ramadan T (1997) Effects of zinc and salinity on growth and anatomical structure of Carthamus tinctorius L. Plant Biol 39:411–418

    Article  CAS  Google Scholar 

  • Glenn EP, Brown JJ (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  • Grigore MN, Toma C, Lacramioara I (2010) Anatomical and ecological observations on Mediterranean halophytes: Suaeda Forssk. ex Scop. genus. Univ Iaşi Rom 54:23–28

    Google Scholar 

  • Grigore MN, Villanueva M, Boscaiu M, Vicente O (2012) Do halophytes really require salts for their growth and development? An experimental approach. Not Sci Biol 4:23–29

    Article  CAS  Google Scholar 

  • Hameed M, Ashraf M, Al-Quriany F, Nawaz T, Ahmad MSA, Younis A, Naz N (2011) Medicinal flora of the Cholistan desert: A review. Pak J Bot 43:39–50

    Google Scholar 

  • Huchzermeyer B, Flowers T (2013) Putting halophytes to work - genetics, biochemistry and physiology. Func Plant Biol 40:5–8

    Article  CAS  Google Scholar 

  • Kader MA, Lindberg S, Seidel T, Golldack D, Yemelyanov V (2007) Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt-tolerant and salt-sensitive rice (Oryza sativa L.) cultivars. Physiol Plant 130:99–111

    Article  CAS  Google Scholar 

  • Khan MA, Ungar IA, Showalter AM (2005) Salt stimulation and tolerance in an intertidal stem-succulent halophyte. J Plant Nutr 28:1365–1374

    Article  CAS  Google Scholar 

  • Kowalenco CG, Lowe LE (1973) Determination of nitrate in soil extracts. Soil Sci Soc Amer Proc 37:660

    Article  Google Scholar 

  • Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228

    Article  CAS  Google Scholar 

  • Li J, Hussain T, Feng X, Guo K, Chen H, Yang C, Liu X (2019) Comparative study on the resistance of Suaeda glauca and Suaeda salsa to drought, salt, and alkali stresses. Ecol Engin 140:105593

    Article  Google Scholar 

  • Lo TY, Cui HZ, Tang PWC, Leung HC (2008) Strength analysis of bamboo by microscopic investigation of bamboo fibre. Construct Build Mat 22:1532–1535

    Article  Google Scholar 

  • Mahmood IA, Salim M, Ali A, Arshadullah M, Zaman B, Mir A (2009) Impact of calcium sulphate and calcium carbide on nitrogen use efficiency of wheat in normal and saline sodic soils. Soil Environ 28:29–37

    CAS  Google Scholar 

  • Marcum KB (1999) Salinity tolerance mechanisms of grasses in the subfamily Chloridoideae. Crop Sci 39:1153–1160

    Article  Google Scholar 

  • McSorley KA, Rutter A, Cumming R, Zeeb BA (2016) Chloride accumulation vs 549 chloride excretion: phytoextraction potential of three halophytic grass species growing in 550 a salinized landfill. Sci Total Environ 572:1132–1137

    Article  CAS  Google Scholar 

  • Naz N, Fatima S, Hameed M, Batool R, Ashraf M, Ahmad F, Ahmad MSA, Naseer M, Zahoor A, Ahmad KS (2016) Adaptive components for salinity tolerance in Sporobolus ioclados (Nees ex Trin.) Nees from the Cholistan Desert, Pakistan. Flora 223:46–55. https://doi.org/10.1016/j.flora.2016.04.013

  • Naz N, Hameed M, Wahid A, Arshad M, Ahmad MSA (2009) Patterns of ion excretion and survival in two stoloniferous arid zone grasses. Physiol Plant 135:185–195

    Article  CAS  Google Scholar 

  • Naz N, Hameed M, Ahmad MSA, Ashraf M, Arshad M (2010) Is soil salinity one of the major determinants of community structure under arid environments? Comm Ecol 11:84–90

    Article  Google Scholar 

  • Naz N, Hameed M, Nawaz T, Ahmad MSA, Ashraf M (2012) Soil-plant relationships in the arid saline desert of Cholistan. Arid Land Res Manag 27:140–152

    Article  Google Scholar 

  • Naz N, Hameed M, Nawaz T, Batool R, Ashraf M, Ahmad F, Ruby T (2013) Structural adaptations in the desert halophyte Aeluropus lagopoides (Linn.) Trin. ex Thw. under high salinity. J Biol Res-Thessalon 19:150–164

    Google Scholar 

  • Naz N, Rafique T, Hameed M, Ashraf M, Batool R, Fatima S (2014) Morpho-anatomical and physiological attributes for salt tolerance in sewan grass (Lasiurus scindicus Henr.) from Cholistan Desert. Pakistan. Acta Physiol Plant 36:2959–2974

    Article  CAS  Google Scholar 

  • Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Func Plant Biol 40:832–847

    Article  CAS  Google Scholar 

  • Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83

    Article  Google Scholar 

  • Rashid P, Ahmed A (2011) Anatomical adaptations of Myriostachya wightiana Hook. f. to salt stress. Dhaka Univ J Biol Sci 20:205–208

    Article  Google Scholar 

  • Razik Abd Al, Husien AHM, Abd Al NabyMahmod DA, Al-Mogasby M, Salam Abd Al (2013) Salinity tolerance of the flora halophytes to coastal habitat of Jarjr-oma in Libya. Nature Sci 11:29–45

    Google Scholar 

  • Rozema J, Schat H (2013) Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ Exp Bot 92:83–95

    Article  CAS  Google Scholar 

  • Ruzin SE (1999) Plant Microtechnique and Microscopy. Oxford University Press, New York, NY, USA

    Google Scholar 

  • Shaar-Moshe L, Blumwald E, Peleg Z (2017) Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat. Plant Physiol 174:421–434

    Article  CAS  Google Scholar 

  • Soil Survey Staff (2004) Soil survey investigations report no. 45, version 2.0, February 2011. Compiled and Edited by Rebecca Burt, United States Department of Agriculture Natural Resources Conservation Service, National Soil Survey Center, Lincoln

  • Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    Article  CAS  Google Scholar 

  • Thorup-Kristensen K, Halberg N, Nicolaisen M, Olesen JE, Crews TE, Hinsinger P, Kirkegaard J, Pierret A, Dresbøll DB (2020) Digging deeper for agricultural resources, the value of deep rooting. Trends Plant Sci 25:406–417

    Article  CAS  Google Scholar 

  • Ungar IA (1991) Ecophysiology of vascular halophytes. CRC Press, Boca Raton, pp 209

  • Waters S, Gilliham M, Hrmova M (2013) Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. Int J Mol Sci 14:7660–7680

    Article  CAS  Google Scholar 

  • Wetson AM, Zörb C, John EA, Flowers TJ (2012) High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis. Ann Bot 109:1027–1036

    Article  CAS  Google Scholar 

  • Wolf B (1982) An improved universal extracting solution and its use for diagnosing soil fertility. Commun Soil Sci Plant Anal 13:1005–1033

    Article  CAS  Google Scholar 

  • Yoshida S (1976) Routine procedure for growing rice plants in culture solution. In: Yoshida S, Forno DA, Cock JH (eds) Laboratory manual for physiological studies of rice. International Rice Research Institute, Los Baños, pp 61–66

  • Younis A, Riaz A, Ikram S, Nawaz T, Hameed M, Fatima S, Batool R, Ahmad F (2013) Salinity-induced structural and functional changes in 3 cultivars of Alternanthera bettzickiana (Regel) G. Nicholson. Turk J Agric For 37:674–687

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Botany, The Islamia University of Bahawalpur, Bahawalpur, Pakistan

    Nargis Naz

  2. Department of Botany, Government Sadiq College Women University, Bahawalpur, Pakistan

    Sana Fatima, Iftikhar Ahmad & Farial Ejaz

  3. Department of Botany, University of Agriculture Faisalabad, Faisalabad, Pakistan

    Mansoor Hameed, Muhammad Sajid Aqeel Ahmad, Farooq Ahmad, Syed Mohsan Raza Shah & Faakeha Islam

  4. Institute of Molecular Biology and Biotechnology, The University of Lahore, Lahore, Pakistan

    Muhammad Ashraf

  5. Department of Botany, Government College Women University, Faisalabad, Pakistan

    Mehwish Naseer

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  1. Nargis Naz
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Contributions

Nargis Naz: This manuscript is derived from the Mphil studies of the first author.

Mansoor Hameed, Muhammad Ashraf, Farooq Ahmad, Iftikhar Ahmad: They are members of the research team supervised the research planning and collection of plant and soil samples.

Muhammad Sajid Aqeel Ahmad: As an statistical expert, he conducted data analysis, visualization and interpretation.

Sana Fatima, Syed Mohsan Raza Shah, Faakeha Islam, Farial Ejaz, Mehwish Naseer: Research execution, biochemical analysis and data collection.

Corresponding author

Correspondence to Mansoor Hameed.

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Naz, N., Fatima, S., Hameed, M. et al. Contribution of structural and functional adaptations of hyper-accumulator Suaeda vera Forssk. ex J.F. Gmel. for adaptability across salinity gradients in hot desert. Environ Sci Pollut Res 29, 64077–64095 (2022). https://doi.org/10.1007/s11356-022-19167-1

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