Elsevier

Plant Physiology and Biochemistry

Volume 132, November 2018, Pages 145-155
Plant Physiology and Biochemistry

Research article
Analysis of physiological traits in the response of Chenopodiaceae, Amaranthaceae, and Brassicaceae plants to salinity stress

https://doi.org/10.1016/j.plaphy.2018.08.040Get rights and content

Highlights

  • Patterns of ion accumulation could be used to discern degrees of salt-tolerance in halophytes.

  • A. halimus maintained turgor with greater growth promotion than in the other halophytes.

  • S. fruticosa maintained a constant L0 and increased the osmotic potential to cope with stress.

  • Patterns of protein and unsaturated fatty acid ratios marked two halophyte responses to salinity.

Abstract

Soil salinity is one of the main factors affecting plant growth. Dissection of plant response to salinity into physiological traits may result a simple approximation than the overall response that may influence many aspects of the plant. In the present study two factors were considered to evaluate the correlation of different physiological variables in the plant response to salinity. The first factor was the species, with four levels (Atriplex halimus, Salicornia fruticosa, Cakile maritima, and Brassica rapa), and the second was the salinity (0, 100, 200, and 300 mM NaCl). Thus, the interrelationships of distinct physiological traits – leaf succulence, minerals (micronutrients and macronutrients), plant water relations (osmotic potential, water potential, and hydraulic conductivity), protein content, catalase, and unsaturated fatty acids - were analyzed by Discriminant Canonical Analysis (DCA). Additional information supplied by the interaction between the variables provided a multivariate response pattern in which the two factors (species x salinity) influenced the relationship between responses rather than affecting a single response. Such analysis allows to establish whether the selected trait was associated to each other for helping to define the best set of parameters in relation to the response of new genotypes to salinity. Thus, plant growth was influenced by leaf succulence adaptation to salt stress whereas it was not determined by water relations. The Na ion prevailed over K as the element with the highest variability in the response to salinity in A. halimus and S. fruticosa, whereas in C. maritima and B. rapa, Ca, S, and P stood out more. Patterns of ion accumulation together with the protein and unsaturated fatty acid ratios could be used in discriminating plant response to salt stress may be positioned in interrelated groups. The results highlight new evidences in the response to salt stress associated to a specific interrelationship of a set of physiological parameters.

Introduction

Saline soils are widespread in many regions of the world due to abundant seawater intrusion in coastal areas, as well as the occurrence of saline groundwater and inadequate irrigation and/or drainage (Souza Filho et al., 2003). Therefore, the possibility of cultivating crops under saline conditions is of high importance in these areas. The breeding of new cultivars is the most common approach to increasing the salt tolerance of crop species (Megdiche et al., 2007). It has been suggested that the salt tolerance of plants could be improved by defining genes or characters for geneticists or breeders to exploit (Munns, 1993). However, salt adjustment mechanisms are complex phenomena, with both biophysical and biochemical implications at different plant levels (Duarte et al., 2014).

Plants have evolved numerous salt tolerance mechanisms to subsist with the damaging effects of salinity. Among these, ion exclusion, adjustment of the cell osmotic potential (Ψπ) (Türkan and Demiral, 2009), and stability of the cell structure and function (Chalbi et al., 2013) are of special importance.

In nature, halophytes are found on the rocky coastlines of the Mediterranean regions and were recently recommended as cash crops for bio-saline agriculture (Ventura et al., 2014). Halophytes grow in very salty soil, and are typically considered as plants able to complete their life cycle in such conditions. In contrast to most glycophytic crops, during their evolution they have not lost their mechanisms of resistance to salt-stress conditions (Koyro and Lieth, 1998). One of these mechanisms is to store the salt ions in the vacuole as osmotica, together with neutral molecules (Belkheiri and Maurizio, 2013). Osmotic adjustment is a mechanism used to preserve turgor and lessen the deadly effects of water stress on vegetative and reproductive tissues. For this, plants are required to keep their hydraulic potential lower than that of the solution surrounding the roots, thereby maintaining turgidity and the uptake of the water necessary for their growth (Flowers et al., 1991). Moghaieb et al. (2004) showed that Suaeda maritima has the ability to maintain osmotic adjustment due to the accumulation of higher solute concentrations in its cells in response to salinity. However, little is known about the interaction between these physiological components.

Also due to salinity, nutrient deficiencies or imbalances in plant tissues occur. Decreases in K, Ca, Mg, and NO3 concentrations have been observed in plants under salinity, a result of the competition of Na and Cl with nutrients (Romero-Aranda et al., 1998). The accumulation of a high Na concentration in the aerial parts is a typical halophytic response (Chalbi et al., 2013).

Changes in the fatty acid content and profile have been reported in some halophytes under salt stress. Thus, the fatty acid composition of Salicornia and Sarcocornia shoots was dominated by 16- and 18-carbon polyunsaturated acids, but a significant amount of saturated acids was also present (Imai et al., 2004; Kulis et al., 2010; Ventura et al., 2011). In Crithmum maritimum a high percentage of palimitic, linoleic, and linolenic acids was observed (Ben Hamed et al., 2005). In addition, an intrinsically high degree of unsaturation in the plasma membrane of the halophyte Cakile maritima, relative to Brassica napus and Brassica oleracea, was considered as a constitutive mechanism to cope with salt stress (Chalbi et al., 2015) and was correlated with lipoxygenase activity. Amongst different halophytes, the proportion of membrane lipids (phospholipids and sterols) and unsaturated fatty acids was correlated to different levels of salt tolerance through the control of permeability and membrane functions (Sui and Guoliang, 2014). In addition, salinity stress can cause oxidative damage to lipids and disturb the cellular metabolism (Anjum et al., 2014). A significant increase in lipid peroxidation in shoots occurred at high salt concentration in halophytes and an elevated antioxidant capacity of halophytes is one of the main reasons of a higher tolerance in relation to glycophytes (Ozgur et al., 2013). Among the antioxidant enzymes to maintain redox status, catalase (CAT) is one of the most efficient in the degradation of H2O2 (Lesser, 2006) and the levels of CAT increased under salt stress in plants and was correlated with salt tolerance (Anjum et al., 2014).

In this work, we select a set of physiological and biochemical parameters to define the responses of one Chenopodiaceae (Atriplex halimus) and one Amaranthaceae (Salicornia fruticosa) and two Brassicaceae (Cakile maritima and Brassica rapa) to salinity. Atriplex halimus, a typically Mediterranean species, is a xero-halophyte (Bendaly et al., 2016), S. fruticosa is a salt marsh euhalophyte (Feng et al., 2015), C. maritima is a highly salt tolerant plant, frequently found on the Mediterranean seashore, where it contributes to sand dune fixation due to its deep root system (Debez et al., 2013), and B. rapa is classified as a tolerant glycophyte (Su et al., 2013).

Previous reports have studied the response of two contrasting genotypes to different levels of salt stress at; transcriptional (Beritognolo et al., 2011), proteomic (Cui et al., 2015) or metabolomics (Zhao et al., 2014). However, but in addition to genotypic information, the potential variability of the particular trait under study must be considered when selecting among a set of physiological parameters. In order to compare the adaptive response to salinity among the four studied species, with the aim of finding the parameter that has most influence within the response to salt stress, a complete study of water relations (root hydraulic conductance (L0), leaf water potential (Ψω), osmolarity of exuded sap (Ψπ), leaf turgor potential (Ψt)) and nutrients (macronutrients (Ca, K, Mg, Na, P, and S) and micronutrients (B, Cu, Fe, Mn, Mo, Ni, and Zn)) was performed. Also, the protein content, double bond index of fatty acids (DBI), and CAT activity were determined. With the objective of obtaining reliable conclusions from the tests performed, and due to the interrelation of the variables, a multivariate statistical technique, namely Multivariate Analysis of Variance (MANOVA) (Daoyu and Lawes, 2000; Johnson et al., 2007), was carried out instead of ANOVA, followed by Discriminant Canonical Analysis (DCA) to interpret the MANOVA (Tatsuoka, 1973).

Section snippets

Plant culture

The Chenopodiaceae (A. halimus), the Amaranthaceae (S. fruticosa), and two Brassicaceae (C. maritima and B. rapa) were chosen for their differing responses to salinity. Plants of A. halimus and S. fruticosa were provided by Viveros Muzalén S.L. (Murcia, Spain). Seeds of C. maritima were collected from Raoued (20 km North of Tunis, Tunisia). Seeds of B. rapa were provided by Sakata Ibérica S.L. (Valencia, Spain). The seeds of C. maritima and B. rapa were sterilized in 0.5% (v/v) sodium

Results and discussion

To study the interrelationships among the four species under the four saline treatments, DCA was used. The two–way MANOVA realised for each group of variables showed that the factors species and salinity were statistically significant, as was their interaction (P < 0.05), for all variables of each group as a whole (Table 1).

Conclusions

There is a complex interaction between the species and salinity that for each variable was resolved to show clear positions of the groups, related to different physiological responses. Thus, leaf succulence was an adaptive mechanism to salt stress related to growth in all species, but a direct correlation between water relations and growth promotion by salinity could not be established. In A. halimus and S. fruticosa, Na ion prevailed over K as a determining element which bypass is determinant

Contributions

María del Carmen Martínez-Ballesta, Lucia Yepes and Najla Chelbi Conception and design Analysis and interpretation of the data.

María del Carmen Martínez-Ballesta and Micaela Carvajal Drafting of the article Critical revision of the article for important intellectual content.

María del Carmen Martínez-Ballesta and Micaela Carvajal Final approval of the article. Provision of study materials.

Juana María Vivo: Article processing, Critical review of the article, Statistical analysis of data.

Manuel

Funding information

This work was partially funded by the Spanish Ministry of Science and Innovation. Project “Retos Colaboración (RTC-2015-3536-2)” FEDER.

Acknowledgements

The authors thank Dr. D. Walker, for correction of the written English in the manuscript.

The authors thank. Prof, Christian Wilhelm for the manuscript comments.

References (71)

  • Y. Himabindu et al.

    Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes

    Environ. Exp. Bot.

    (2016)
  • M.B. Jackson et al.

    Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants

    Ann. Bot.

    (1996)
  • L. López-Pérez et al.

    Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity

    Phytochemistry

    (2009)
  • R.E.A. Moghaieb et al.

    Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritima

    Plant Sci.

    (2004)
  • B. Nedjimi

    Effects of salinity on growth, membrane permeability and root hydraulic conductivity in three saltbush species

    Biochem. Systemat. Ecol.

    (2014)
  • J. Rozema et al.

    Effect of elevated atmospheric Co2 on growth, photosynthesis and water relations of salt-marsh grass species

    Aquat. Bot.

    (1991)
  • J. Rozema et al.

    Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture

    Environ. Exp. Bot.

    (2013)
  • Y. Ventura et al.

    Effect of seawater concentration on the productivity and nutritional value of annual Salicornia and perennial Sarcocornia halophytes as leafy vegetable crops

    Sci. Hortic. (Amsterdam)

    (2011)
  • D. Wang et al.

    Sodium instead of potassium and chloride is an important macronutrient to improve leaf succulence and shoot development for halophyte Sesuvium portulacastrum

    Plant Physiol. Biochem.

    (2012)
  • A. Amanullah

    Specific leaf area and specific leaf weight in small grain crops wheat, rye, barley, and oats differ at various growth stages and NPK source

    J. Plant Nutr.

    (2015)
  • N.A. Anjum et al.

    Understanding stress-responsive mechanisms in plants: an overview of transcriptomics and proteomics approaches

  • N.A. Anjum et al.

    Glutathione and proline can coordinately make plants withstand the joint attack of metal(loid) and salinity stresses

    Front. Plant Sci.

    (2014)
  • O. Belkheiri et al.

    Effect of water stress on growth, water use efficiency and gas exchange as related to osmotic adjustment of two halophytes Atriplex spp

    Funct. Plant Biol

    (2013)
  • N. Ben Amor et al.

    The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress

    Acta Physiol. Plant.

    (2010)
  • I. Beritognolo et al.

    Comparative study of transcriptional and physiological responses to salinity stress in two contrasting Populus alba L. genotypes

    Tree Physiol.

    (2011)
  • F. Boughalleb et al.

    Anatomical changes induced by increasing NaCl salinity in three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea

    Acta Physiol. Plant.

    (2009)
  • N. Chalbi et al.

    Are changes in membrane lipids and fatty acid composition related to salt-stress resistance in wild and cultivated barley?

    J. Plant Nutr. Soil Sci.

    (2013)
  • G. Clausing et al.

    Historical biogeography in a linear system: genetic variation of sea rocket (Cakile maritima) and sea holly (Eryngium maritimum) along European coasts

    Mol. Ecol.

    (2000)
  • D. Cui et al.

    Proteomic analysis of seedling roots of two maize inbred lines that differ significantly in the salt stress response

    PLoS One

    (2015)
  • Z. Daoyu et al.

    Manova and discriminant analyses of phenotypic data as a guide for parent selection in kiwifruit (Actinidia deliciosa) breeding

    Euphytica

    (2000)
  • A.B. Das et al.

    Salinity-induced genes and molecular basis of salt-tolerant strategies in mangroves

  • A.J. Davy et al.

    Population differentiation in the life-history characteristics of salt-marsh annuals

    Vegetatio

    (1985)
  • B. Duarte et al.

    Biophysical and biochemical constraints imposed by salt stress: learning from halophytes

    Front. Plant Sci.

    (2014)
  • T.P. Egan et al.

    The effect of different salts of sodium and potassium on the accumulation of glycinebetaine in Atriplex prostrata

    Biol. Plant. (Prague)

    (2001)
  • J. Feng et al.

    High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea

    BMC Plant Biol.

    (2015)
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