Abstract
In this study, pepper (Capsicum annuum L.) inbred lines were grafted onto different rootstock genotypes and tested under saline conditions. A hydroponic experiment was conducted in nutrient solution growth system in a growth chamber of Erciyes University, Agricultural Faculty in Kayseri, Turkey. The experiment was conducted in spring 2017 growth season. Two pepper inbred lines (ERÜ-462 and ERÜ-1227) were grafted onto three different pepper rootstocks/genotypes (Scarface F1, 11B14, and Yaocali F1) and grown in 8 L pots filled with continuously aerated nutrient solution under saline conditions (8 dS m−1) with three replications. The growth chamber experiment was carried out to determine the effects of salt stress on plant growth, shoot and root dry weights, leaf area, photosynthesis, leaf total chlorophyll (a + b) and carotenoid content, proline content, glycine betaine content, leaf electrolyte leakage, leaf and root macro element concentration in grafted and non-grafted pepper plants. The results indicated that ERÜ-462 grafted on to Scarface and 11B14 rootstock genotypes were more tolerant to salinity than ERÜ-1227 in term of leaf chlorophyll (a + b) content and leaf carotenoid content, photosynthesis, and proline content. Though, higher shoot and root biomass, leaf area formation, root K+, Na+, Cl− contents were observed when ERÜ-1227 grafted on to Scarface and 11B14 rootstock genotypes. Strong rootstock promoted plant growth in pepper plant both under control and saline conditions and significant depression of plant biomass production under saline conditions was observed in both grafted and non-grafted plants. However, grafting onto vigorous rootstocks alleviated negative effects of salinity stress on pepper plants. Scarface and 11B14 were found more tolerant to salinity than non-grafted pepper plants and the other genotypes used as regard to investigated parameters.
Zusammenfassung
In dieser Studie wurden Paprika-Inzuchtlinien (Capsicum annuum L.) auf verschiedene Wurzelstockgenotypen gepfropft und unter salzhaltigen Bedingungen getestet. Ein hydroponisches Experiment wurde in einem Nährlösungs-Wachstumssystem in einer Wachstumskammer der Erciyes-Universität der Landwirtschaftlichen Fakultät in Kayseri, Türkei, durchgeführt. Das Experiment fand in der Wachstumssaison im Frühjahr 2017 statt. Zwei Paprika-Inzuchtlinien (ERÜ-462 und ERÜ-1227) wurden auf drei verschiedene Wurzelstöcke (Scarface F1, 11B14 und Yaocali F1) gepfropft und in 8‑Liter-Töpfen, die mit kontinuierlich belüfteter Nährlösung gefüllt waren, unter salzhaltigen Bedingungen (8 dS m−1) angebaut; das Experiment wurde drei Mal wiederholt. Das Wachstumskammerexperiment wurde durchgeführt, um die Auswirkungen von Salzstress auf das Pflanzenwachstum, das Spross- und Wurzeltrockengewicht, die Blattfläche, die Photosynthese, den Gesamtchlorophyll- (a + b) und Carotinoidgehalt, den Prolingehalt, den Glycinbetaingehalt, den Elektrolytverlust des Blatts und die Konzentration von Blatt- und Wurzel-Makroelementen bei gepfropften und nicht gepfropften Paprikapflanzen zu bestimmen. Die Ergebnisse zeigten, dass ERÜ-462, das auf Scarface- und 11B14-Wurzelstock-Genotypen gepfropft wurde, hinsichtlich des Blattchlorophyllgehalts und des Blattcarotinoidgehalts, der Photosynthese und des Prolingehalts salztoleranter war als ERÜ-1227. Allerdings wurden höhere Spross- und Wurzelbiomasse, Blattflächenbildung, Wurzel‑K+-, -Na+- und -Cl−-Gehalte beobachtet, wenn ERÜ-1227 auf Scarface- und 11B14-Wurzelstock-Genotypen gepfropft wurde. Ein starker Wurzelstock förderte das Pflanzenwachstum der Paprikapflanzen sowohl unter Kontroll- als auch unter salzhaltigen Bedingungen und eine signifikante Verringerung der Pflanzenbiomasseproduktion unter salzhaltigen Bedingungen wurde sowohl bei gepfropften als auch bei nicht gepfropften Pflanzen beobachtet. Das Pfropfen auf kräftige Wurzelstöcke milderte jedoch die negativen Auswirkungen von Salzstress auf Paprikapflanzen Scarface und 11B14 erwiesen sich in Bezug auf die untersuchten Parameter als salztoleranter als nicht gepfropfte Paprikapflanzen und die anderen verwendeten Genotypen.
Similar content being viewed by others
References
Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59(15):4119–4131
Almeida P, Feron R, de Boer G, de Boer A (2014) Role of Na+, K+, Cl−, proline and sucrose concentrations in determining salinity tolerance and their correlation with expression of multiple genes in tomato. AoB Plants. https://doi.org/10.1093/aobpla/plu039
Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16
Awang YB, Atherton JG, Taylor AJ (1993) Salinity effects of strawberry plants grown in rockwool I. Growth and leaf water relations. J Hortic Sci 68:783–790
Bai LP, Zhou BL, Li N, Huo SF, Fu YW (2005) The ion absorption and transportation of grafted eggplants (Solanum melongena L.) under NaCl stress. Plant Physiol Commun 41:767–769
Balal RM, Ashraf MY, Khan MM, Jaskani MJ, Ashfaq M (2011) Influence of salt stress on growth and biochemical parameters of citrus rootstocks. Pak J Bot 43:2135–2141
Bandeoglu E, Eyidogan F, Yucel M, Oktem HA (2004) Antioxidant responses of shoots and roots of lentil to NaCl-salinity stress. Plant Growth Regul 42:69–77
Bates LS, Waldren RP, Tevre IU (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Bavei V, Shiran B, Arzani A (2011) Evaluation of salinity tolerance in sorghum (Sorghum bicolor L.) using ion accumulation, proline and peroxidase criteria. Plant Growth Regul 64:275–285
Bethke PC, Drew MC (1992) Stomatal and nonstomatal components to inhibition of photosynthesis in leaves of Capsicum annuum during progressive exposure to NaCl salinity. Plant Physiol 99:219–226
Blanco-Ríos AK, Medina-Juárez LÁ, González-Aguilar GA, Gámez-Meza N (2013) Antioxidant activity of the phenolic and oily fractions of different sweet bell peppers. J Mex Chem Soc 57:137–143
Bojórquez-Quintal E, Velarde-Buendía A, Ku-González Á, Carillo-Pech M, Ortega-Camacho D, Echevarría-Machado I, Pottosin I, Martínez-Estévez M (2014) Mechanisms of salt tolerance in habanero pepper plants (Capsicum chinense Jacq.): proline accumulation, ions dynamics and sodium root-shoot partition and compartmentation. Front Plant Sci 5:605
Cevik B (1986) Soil water protection engineering. Agriculture Faculty Press number: 108. Çukurova University, Adana (in Turkish)
Chartzoulakis K, Klapaki G (2000) Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages. Sci Hortic 86:247–260
Chartzoulakis K, Loupassaki MH (1997) Effects of NaCl salinity on germination, growth, gas exchange, and yield of greenhouse eggplant. Agric Water Manag 32:214–225
Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58:4245–4255
Colla G, Rouphael Y, Cardarelli M, Rea E (2006) Effect of salinity on yield, fruit quality, leaf gas exchange, and mineral composition of grafted watermelon plants. HortScience 41:622–627
Colla G, Rouphael Y, Leonardi C, Bie Z (2010) Role of grafting in vegetable crops grown under saline conditions. Sci Hortic 127:147–155
Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45:1425–1443
Dasgan HY, Aktas H, Abak K, Cakmak I (2002) Determination of screening techniques to salinity tolerance in tomato and investigation of genotypes responses. Plant Sci 163:695–703
Davis AR, Perkins-Veazie P, Sakata Y, López-Galarza S, Maroto JV, Lee SG et al (2008) Cucurbit grafting. CRC Crit Rev Plant Sci 27:50–74
De Pascale S, Barbieri G (1997) Effects of salinity and top removal on growth and yield of broad bean as a green vegetable. Sci Hortic 71:147–165
De Pascale S, Ruggiero C, Barbieri G (2003) Physiological responses of pepper to salinity and drought. J Am Sociol Hortic Sci 128:48–54
Dumbroff EB, Cooper A (1974) Effects of salt stress applied in balanced nutrient solutions at several stages during growth of tomato. Bot Gaz 135:219–224
Etehadnin M, Schoenau J, Waterer D, Karen T (2010) The effect of CaCl2 and NaCl salt acclimation in stress tolerance and its potential role in ABA and scion/rootstock-mediated salt stress responses. Plant Stress 4:72–81
Ferreira-Silva SL, Silva EN, Carvalho FEL, de Lima CS, Alves FAL, Silveira JAG (2010) Physiological alterations modulated by rootstock and scion combination in cashew under salinity. Sci Hortic 127:39–45
Fischer TR, Byerlee D, Edmeades GO (2011) Can technology deliver on the yield challenge to 2050? In: Conforti P (ed) Looking ahead in world food and agriculture: perspectives to 2050. Economic and Social Development Department, FAO, Rome, pp 389–462
Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C(3) plants. Plant Biol 6:269–279
Garriga M, Munoz CA, Caligari PDS, Retamales JB (2015) Effect of salt stress on genotypes of commercial (Fragaria X ananassa) and Chilean strawberry (F. chiloensis). Sci Hortic 195:37–47
Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot 47:39–50
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Giuffrida F, Cassaniti C, Leonardi C (2013) The influence of rootstock on growth and ion concentrations in pepper (Capsicum annuum L.) under saline conditions. J Hortic Sci Biotechnol 88:110–116
Gong B, Wen D, VandenLangenberg K, Wei M, Yang F, Shi Q, Wang X (2013) Comparative effects of NaCl and NaHCO3 stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic 157:1–12
Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190
Grieve CM, Grattan SR (1983) Rapid assay for the determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
Gungor B, Balkaya A (2016) The quantitative effects of local pumpkin rootstock candidates on the vegetative growth of grafted mini watermelon. Bahçe 2:21–26 (in Turkish)
Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate saltinduced damages. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949
Hmidi D, Abdelly C, Athar HR, Ashraf M, Messedi D (2018) Effect of salinity on osmotic adjustment, proline accumulation and possible role of ornithine-δ-aminotransferase in proline biosynthesis in Cakile maritima. Physiol Mol Biol Plants 24(6):1017–1033. https://doi.org/10.1007/s12298-018-0601-9
Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00080
Johnson CM, Ulrich A (1959) Analytical methods for use in plant analysis, 1st edn. California Agricultural Experiment Station, Berkeley
Kaya C, Kirnak H, Higgs D (2001) Enhancement of growth and normal growth parameters by foliar application of potassium and phosphorus on tomato cultivars grown at high (NaCl) salinity. J Plant Nutr 24:357–367
Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189:54–81
Kumar K, Kumar M, Kim SR, Ryu H, Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6:1–15
Kurunc A, Unlukara A, Cemek B (2011) Salinity and drought affect yield response of bell pepper similarly. Acta Agric Scand B Soil Plant Sci 61:514–522
Li H, Chang J, Chen H, Wang Z, Gu X, Wei C, Zhang Y, Ma J, Yang J, Zhang X (2017) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front Plant Sci 8:295
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice varieties differing in salinity resistance. J Exp Bot 46:1843–1852
Lycoskoufis IH, Savvas D, Mavrogianopoulos G (2005) Growth, gas exchange and nutrient status in pepper (Capsicum annuum L.) grown in recirculating nutrient solution as affected by salinity imposed to half of the root system. Sci Hortic 106(2):147–161
Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462
Mumtaz-Khan M, Ruqaya S, Al-Mas’oudi M, Al-Said F, Khan I (2013) Salinity effects on growth, electrolyte leakage, chlorophyll content and lipid peroxidation in cucumber (Cucumis sativus L.). In: Int. Conf. Food Agric. Sci, vol 55, pp 28–32
Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218. https://doi.org/10.1023/A:1024553303144
Navarro JM, Garrido C, Carvajal M, Martínez V (2002) Yield and fruit quality of pepper plants under sulphate and chloride salinity. J Hortic Sci Biotechnol 77:52–57
Olías R, Eljakaoui Z, Li J, De Morales PA, Marín-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32(7):904–916
Özdemir B, Tanyolac ZÖ, Ulukapı K, Onus AN (2016) Evaluation of salinity tolerance level of some pepper (Capsicum annuum L.) cultivars. Int J Agric Innov Res 5(2):247–251
Öztekin GB (2009) Effects of rootstocks on grafted tomato plants under salt stress. Master Thesis. Ege University, Graduate School of Natural and Applied Sciences, Izmir
Penella C, Landi M, Guidi L, Nebauer SG, Pellegrini E, Bautista AS, Remorini D, Nali C, López-Galarza S, Calatayud A (2016) Salt-tolerant rootstock increases yield of pepper under salinity through maintenance of photosynthetic performance and sinks strength. J Plant Physiol. https://doi.org/10.1016/j.jplph.2016.02.007
Penella C, Nebauer SG, Bautista AS, López-Galarza S, Calatayud A (2014) Rootstock alleviates PEG-induced water stress in grafted pepper seedlings: physiological responses. J Plant Physiol 171:842–851
Penella C, Nebauer SG, Lopez-Galarza S, Oliver AQ (2017) Grafting pepper onto tolerant rootstocks: an environmental-friendly technique overcome water and salt stress. Sci Hortic 226:33–41
Penella C, Nebauer SG, Quiñones A, Bautista AS, López-Galarza S, Calatayud A (2015) Some rootstocks improve pepper tolerance to mild salinity through ionic regulation. Plant Sci 230:12–22
Perez-Lopez U, Robredo A, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2008) The impact of salt stress on the water status of barley plants is partially mitigated by elevated CO2. Environ Exp Bot 66(3):463–470
Pogonyi Á, Pé KZ, Helyes L, Lugasi A (2005) Effect of grafting on the tomato’s yield, quality and main fruit components in spring forcing. Acta Aliment 34:453–462
Radic S, Stefanic PP, Lepedus H, Roje V, Pevalek-Kozlina B (2013) Salt tolerance of Centaurea ragusina L. is associated with efficient osmotic adjustment and increased antioxidative capacity. Environ Exp Bot 87:39–48
Ramoliya PJ, Patel HM, Joshi JB, Pandey AN (2006) Effect of salinization of soil on growth and nutrient accumulation in seedlings of Prosopis cineraria. J Plant Nutr 29:283–303
Rao A, Ahmad SD, Sabir SM, Awan SI, Shah AH, Abbas SR, Shafique S, Khan F, Chaudhary A (2013) Potential antioxidant activities improve salt tolerance in ten varieties of wheat (Triticum aestivum L.). AJPS 4:69–76
Rengel Z (1992) The role of calcium in salt toxicity. Plant Cell Environ 15:625–632
Romero L, Belakbir A, Ragala L, Ruiz MJ (1997) Response of plant yield and leaf pigments to saline conditions: effectiveness of different rootstocks in melon plant (Cucumis melo L.). Soil Sci Plant Nutr 43:855–862
Rouphael Y, Cardarelli M, Rea E, Colla G (2012) Improving melon and cucumber photosynthetic activity, mineral composition, and growth performance under salinity stress by grafting onto Cucurbita hybrid rootstocks. Photosynthetica 50(2):180–188
Ruggiero A, Landi S, Punzo P, Possenti M, Van Oosten MJ, Costa A, Morelli G, Maggio A, Grillo S, Batelli G (2019) Salinity and ABA seed responses in pepper: expression and interaction of ABA core signaling components. Front Plant Sci 10:304
Saeed R, Mirza S, Ahmad R (2014) Electrolyte leakage and relative water content as affected by organic mulch in okra plant (Abelmoschus esculentus L. Moench) grown under salinity. FUUAST J Biol 4(2):221–227
Sarabi B, Bolandnazar S, Ghaderi N, Ghashghaie J (2017) Genotypic differences in physiological and biochemical responses to salinity stress in melon (Cucumis melo L.) plants: prospects for selection of salt tolerant landraces. Plant Physiol Biochem 119:294–311
Serrano LL, Penella C, San Bautista A, Galarza SL, Chover AC (2017) Physiological changes of pepper accessions in response to salinity and water stress. Spanish J Agric Res 15:15
Sönmez B (1990) Soils with salinity and sodium vol 62. T.O.K.B Research Institute of Rural Services Press, Sanliurfa, Turkey
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Ulas F (2019) Effects of rootstocks with vigorous root system on plant growth, seed yield and quality of pepper (Capsicum annuum L.) inbred lines. Ph.D Thesis. Erciyes University, Graduate School of Natural and Applied Sciences, Kayseri
Ulas A, Aydin A, Ulas F, Yetisir H, Miano TF (2020) Cucurbita rootstocks improve salt tolerance of melon scions by inducing physiological, biochemical and nutritional responses. Horticulturae 6:66
Ulas F, Aydın A, Ulas A, Yetisir H (2019a) Grafting for sustainable growth performance of melon (Cucumis melo) under salt stressed hydroponic condition. Eur J Sustain Dev 8:201–210
Ulas F, Fricke F, Stützel H (2019b) Leaf physiological and root morphological parameters of grafted tomato plants drought stress conditions. Fresenius Environ Bull 28(4A):3423–3434
Upreti KK, Murti GSR (2010) Response of grape rootstocks to salinity: changes in root growth, polyamines and abscisic acid. Biol Plant 54:730–734
Wang Q, Wu C, Xie B, Liu Y, Cui J, Chen G, Zhang Y (2012) Model analyzing the antioxidant responses of leaves and roots of switchgrass to NaCl-salinity stress. Plant Physiol Biochem 58:288–296
Wen JF, Gong M, Liu Y, Hu JL, Deng MH (2013) Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci Hortic 164:366–371
Wignarajah K, Jennings DH, Handley JF (1975) The effect of salinity on growth of Phaseolus vulgaris L. I. Anatomical changes in the first trifoliate leaf. Ann Bot 39:1029–1038
Wu H (2018) Plant salt tolerance and Na+ sensing and transport. Crop J 6:215–225
Wu GQ, Wang SM (2012) Calcium regulates K+/Na+ homeostasis in rice (Oryza sativa L.) under saline conditions. Plant Soil Environ 58:121–127
Wu GQ, Liang N, Feng RJ et al (2013) Evaluation of salinity tolerance in seedlings of sugar beet (Beta vulgaris L.) cultivars using proline, soluble sugars and cation accumulation criteria. Acta Physiol Plant 35:2665–2674
Yakıt S, Tuna A (2006) Tuz stresi altındaki mısır bitkisinde (Zea mays L.) stres parametreleri üzerine Ca, Mg ve K’nın etkileri. Akdeniz Üniv Ziraat Fak Derg 19(1):59–67
Yamac M (2017) Rootstock potential of some selected bottle gourd (Lagenaria Siceraria) genotypes from Turkish germplasm for watermelon under saline conditions. Master Thesis. Erciyes University, Graduate School of Natural and Applied Sciences, Kayseri
Yan Y, Wang S, Wei M, Gong B, Shi Q (2018) Effect of different rootstocks on the salt stress tolerance in watermelon seedlings. Hortic Plant J 4(6):239–249
Yarsi G, Sıvacı A, Dasgan HY, Altuntas O, Binzet R, Akhoundnejad Y (2017) Effects of salinity stress on chlorophyll and carotenoid contents and stomata size of grafted and ungrafted Galia C8 melon cultivar. Pak J Bot 49(2):421–426
Yarsi G, Sari N (2006) Effects of grafted seedling on nutritional status of melon growing in greenhouse. Alatarım 5(2):1–8
Zhen A, Bie Z, Huang Y, Liu Z, Li Q (2010) Effects of scion and rootstock genotypes on the anti-oxidant defense systems of grafted cucumber seedlings under NaCl stress. Soil Science and Plant Nutrition 56(2):263–271
Zhiping H, Shirong G, Yansheng J, Huaifu F, Jun L (2008) Effect of NaCl stress on growth and photosynthetic gas exchange of watermelon seedlings. Acta Botanica Boreali-Occidentalia Sinica 28(4):745–751
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
O. Abidalrazzaq Musluh Al Rubaye, H. Yetisir, F. Ulas and A. Ulas declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Abidalrazzaq Musluh Al Rubaye, O., Yetisir, H., Ulas, F. et al. Enhancing Salt Stress Tolerance of Different Pepper (Capsicum annuum L.) Inbred Line Genotypes by Rootstock with Vigorous Root System. Gesunde Pflanzen 73, 375–389 (2021). https://doi.org/10.1007/s10343-021-00564-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10343-021-00564-4