Research articlePhysiological characterization of a pepper hybrid rootstock designed to cope with salinity stress
Introduction
New scenarios due to climatic change are affecting crop yield and quality. In this context, salinity is one of the most important environmental factors that limits plant growth, productivity, quality and the increasing demand for food crops (Ashraf, 2004; Srivastava and Kumar, 2015). More than 20% of cultivated land worldwide is affected by salt stress and this amount is increasing daily (Srivastava and Kumar, 2015). At the same time, the global population is expected to reach 9 billion by 2050. Thus increasing of agriculture productivity will be needed to meet food demands (Shelden and Roessner, 2013). To achieve the increased food production under salinity conditions, it is necessary to identify naturally occurring genetic variations within a crop species by screening varieties, wild genotypes and landraces that could provide salt tolerance (Roy et al., 2011).
Pepper is an important crop that grows in most countries on our planet, and covers 1.93 million ha of crop-growing surface area (Penella and Calatayud, 2018). As a spice and fruit, the world's pepper production was 34 million tons in 2017 (Penella and Calatayud, 2018). Generally speaking, commercial pepper varieties need friable, well-drained, sandy loam soil with a pH of 6.5–7.5 for optimum production. Salt content in soil and irrigation water should be low. There are reports of a salinity resistance threshold of 1.5 dS m−1, below which no effect on growth occurs, and a 14% drop in biomass production per additional 1 dS m−1 has been reported (Maas, 1973). Pepper and Capsicum annuum species in particular are highly susceptible to salt stress by showing blossom end rot (BER), lower yields and more unmarketable fruits (Penella et al., 2015). Physiological changes have been analyzed in pepper under salt stress like membrane permeability and water channel activity alterations, ion imbalance, reduced total photosynthesis and stomatal conductance, and increasing reactive oxygen species production, which modify the carbon balance required to maintain both productivity and growth (Penella and Calatayud, 2018).
To minimize salinity damage in pepper crops, graft technology is an agronomic practice that can improve plant tolerance by using rootstocks capable of reducing the negative effect of external stress on the scion. In addition, grafted plants can avoid the problem associated with the “building or design” of tolerant varieties due to complexity of salinity traits and lack of practical selection tools; one example is genetic markers, which have made these tasks slow and inefficient (Flowers, 2004; Ashraf and Foolad, 2007; Schwarz et al., 2010). Grafting can combine suitable commercial fruit quality characteristics and high production of a scion and tolerance traits to environmental factors from rootstock by working together like a single plant. Nevertheless, rootstocks that tolerate salt stress are not used in pepper plants because available commercial rootstocks offer limited profits (Lee et al., 2010; Penella et al., 2013; Kyriacou et al., 2017).
There is a need to perform rigorous screenings to find Capsicum plants that tolerate salt stress so they can be used as pepper rootstocks. In this context, we screened physiological and phenotypically characterized accessions of pepper from gene banks before selecting those for their tolerance to salinity and then using them as rootstocks in grafted pepper plants (Penella et al., 2013, 2015; López-Serrano et al., 2017; Penella and Calatayud, 2018). The obtained results have allow to confirm that the tolerance to salinity of these grafted plants was expressed by maintaining scions presenting better physiological performance and, consequently, by increasing yields (Penella et al., 2015, 2016, 2017). Afterward, a classic breeding program was applied to salinity-tolerant pepper accessions (C. annuun x C. annuun) have allowed obtain more uniform hybrids in terms of germination, growth and highest vigor to be used as rootstocks under salinity conditions. One of them, NIBER®, has been tested under real salinity field conditions for several years (Calatayud et al., 2016) and showed higher yields (range of 32%–80%) than ungrafted plants or other tested commercial pepper rootstocks.
The aim of the present work was to evaluate the early physiological response of a tolerant rootstock under salt stress conditions using the hybrid NIBER®. To date, information about the initial mechanisms involved in the tolerance to of grafted pepper plants remains limited. The initial evaluation of root-shoot to physiological evolution is a basic requirement to help develop improved efficient rootstocks with the ability to cope with salinity and to ensure a better understanding of the response mechanisms of grafted pepper plants to imbalanced salinity.
To fulfill this objective, we compared the relative tolerance responses of ungrafted, self-grafted, grafted and reciprocal grafted pepper plants under both control and salinity conditions. Gas exchange, proline, phenols, hydrogen peroxide, radical scavenging capacity and nitrate reductase activity were measured in the leaves of all the pepper plants combinations. Na+/K+, Cl− concentration and ABA levels were determined in both leaves and roots. In addition, biomass parameters (stem and root length and total dry weight) were measured. All those information has been analyzed to identify the mechanisms by which the NIBER® rootstock enhances tolerance to salinity.
Section snippets
Plant material
A new hybrid pepper salinity-tolerant rootstock, NIBER® (Capsicum annuum x C. annuum) (abbreviated herein as N), and the salt-sensitive pepper cultivar ‘Adige’ (abbreviated as A) (Lamuyo type, Sakata Seeds, Japan), were used as either a scion or rootstock. Four plant combinations were herein used: ungrafted A plants (A), self-grafted A plants (A/A), A grafted onto N (A/N) and N grafted onto A (N/A). Early in March, the seeds of A and N were sown in 96 seedling trays filled with a peat-based
Ions determination
The Na+/K+ ratio at the end of experiment (10DAT) was higher in roots than in leaves for all the plant combinations and treatments (Fig. 1). In leaves, Na+/K+ significantly decreased (P < 0.05) in the A/N plants under salt applications (Fig. 1A). Under the control conditions of leaves, A/N showed a decrease with significant differences compared to N/A (Fig. 1A). In the root compartment (Fig. 1B), the Na+/K+ values increased in all the plant combinations under salt treatment. Na+/K+ were
Discussion
Vegetable grafting is an effective technique in increasing salt tolerance (Colla et al., 2010). Some rootstocks, mainly hybrids for tomato, melon and cucumber, have demonstrated tolerance to salinity (Colla et al., 2006; Savvas et al., 2011; Huang et al., 2013). To date, grafting onto pepper rootstocks has not been a feasible solution to cope with salinity given the unsatisfactory performance of available rootstocks (Kyriacou et al., 2017; Penella and Calatayud, 2018). In previous field studies
Authors'contributions
LLS, CP and AC conceived and designed the experiments. LLS, GCS, GVS, CP and AC performed the experiments. AS, SLG, LLS and AC analyzed the data and discussed the study results. AC and SLG wrote the paper. All the authors read and approved the manuscript.
Funding
This work was financed by INIA (Spain) and Ministerio de Ciencia, Innovación y Universidades through Project RTA2017-00030-C02-00 and the European Regional Development Fund (ERDF). L. L-S is a beneficiary of a doctoral fellowship (FPI-INIA).
References (95)
Some important physiological selection criteria for salt tolerance in plants
Flora
(2004)- et al.
Roles of glycine betaine and proline in improving plant abiotic stress resistance
Environ. Exp. Bot.
(2007) - et al.
Some prospective strategies for improving crop salt tolerance
Adv. Agron.
(2008) - et al.
Use of a free radical method to evaluate antioxidant activity
Lebensm. Wiss. Technol.
(1995) - et al.
Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages
Sci. Hortic.
(2000) - et al.
Role of grafting in vegetable crops grown under saline conditions
Sci. Hortic.
(2010) - et al.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
Plant Physiol. Biochem.
(2010) - et al.
Nitrate reductase from higher plants
Methods Enzymol.
(1971) - et al.
Advances in flavonoid research since 1992
Phytochemistry
(2000) - et al.
Grafting increases the salt tolerance of tomato improvement of photosynthesis and enhancement of antioxidant enzymes activity
Environ. Exp. Bot.
(2009)
Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation
Arch. Biochem. Biophys.
Improving the fruit yield and quality of cucumber by grafting onto the salt tolerant rootstock under NaCl stress
Sci. Hortic.
Reciprocal grafting between cucumber and pumpkin demonstrates the roles of the rootstock in the determination of cucumber salt tolerance and sodium accumulation
Sci. Hortic.
Current status of vegetables grafting: diffusion, grafting techniques, automation
Sci. Hortic.
Leaf dehydration is needed to induce abscisic acid accumulation in roots of citrus plants
Environ. Exp. Bot.
Transmissible salt tolerance traits identified through reciprocal grafts between sensitive Carrizo and tolerant Cleopatra citrus genotypes
J. Plant Physiol.
Hydrogen peroxide signalling
Curr. Opin. Plant Biol.
Salt tolerance and salinity effects on plants: a review
Ecotoxicol. Environ. Saf.
Some rootstocks improve pepper tolerance to mild salinity through ionic regulation
Plant Sci.
Salt-tolerant rootstock increases yield of pepper under salinity through maintenance of photosynthetic performance and sinks strength
J. Plant Physiol.
Grafting pepper onto tolerant rootstocks: an environmental-friendly technique overcomes water and salt stress
Sci. Hortic.
Genetic analysis of stress tolerance in crops
Curr. Opin. Plant Biol.
The rootstock effect on the tomato salinity response depends on the shoot genotype
Plant Sci.
Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants
Sci. Hortic.
Proline: a multifunctional amino acid
Trends Plant Sci.
Modelling uptake of Na+ and Cl− by tomato in closed-cycle cultivation systems as influenced by irrigation water salinity
Agric. Water Manag.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants Protective role of exogenous polyamines
Plant Sci.
Plant salt tolerance
Trends Plant Sci.
Effects of grafting on watermelon plant growth, yield and quality
J. Agronomy
Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato
Plant Cell Environ.
Tomato fruit quality as influenced by salinity and nitric oxide
Turk. J. Bot.
Characteristics of the uptake mechanism of chloride ions in excised roots of a woody plant (Citrus)
Physiol. Plant.
Proline accumulation in leaves of Periploca sepium via both biosynthesis up-regulation and transport during recovery from severe drought
PLoS One
Rapid determination of free proline for water stress studies
Plant Soil
ROS as key players in plant stress signalling
J. Exp. Bot.
ROS homeostasis in halophytes in the context of salinity stress tolerance
J. Exp. Bot.
Comportamiento agronómico en condiciones salinas de plantas de pimiento injertadas sobre un nuevo patrón
Agrícola Vergel
Control of plant growth resides in the shoot, and not in the root, in reciprocal grafts of flacca and wild-type tomato (Lysopersicon esculentum), in the presence and absence of salinity stress
Plant Soil
Effect of salinity on yield, fruit quality, leaf gas exchange, and mineral composition of grafted watermelon plants
Hortscience
Grafting cucumber plants enhance tolerance to sodium chloride and sulfate salinization
Sci. Hortic.
Root signals and the regulation of growth and development of plants in drying soil
Annu. Rev. Plant Physiol. Plant Mol. Biol.
Effects of NaCl and proline on polyphenol oxidase activity in bean seedlings
Biol. Plant.
Leaf Senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase
J. Exp. Bot.
Sodium and chloride exclusion and retention by non-grafted and grafted melon and Cucurbita plants
J. Exp. Bot.
Scion and rootstock effects on ABA mediated plant growth regulators and salt tolerance of acclimated and unacclimated potato genotypes
J. Plant Growth Regul.
Leaf phenolic content of some squash rootstocks used on watermelon (Citrullus lanatus (thunb.) Matsum and Nakai) growing and phenolic accumulation on grafted cultivar
Afr. J. Agric. Res.
Effect of salinity on growth, mineral composition, and water relations of grafted tomato plants
J. Plant Nutr. Soil Sci.
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