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Plant function and evolutionary biology
RESEARCH ARTICLE

Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism

Francesco Orsini A , Mattia Accorsi A , Giorgio Gianquinto A , Giovanni Dinelli A , Fabiana Antognoni B , Karina B. Ruiz Carrasco C , Enrique A. Martinez D E , Mohammad Alnayef A , Ilaria Marotti A , Sara Bosi A and Stefania Biondi A F
+ Author Affiliations
- Author Affiliations

A Dipartimento di Scienze e Tecnologie Agroambientali, (DiSTA), Università di Bologna, viale Fanin 44, 40127 Bologna, Italy.

B Dipartimento di Biologia Evoluzionistica Sperimentale, Università di Bologna, via Irnerio 42, 40126 Bologna, Italy.

C Dipartimento di Colture Arboree, Università di Bologna, viale Fanin 44, 40127 Bologna, Italy.

D Centro de Estudios Avanzados en Zonas Aridas (CEAZA), Av. Raúl Bitrán s/n, La Serena, Chile.

E Applied Biology and Ecology, Universidad Catolica del Norte, Coquimbo, Chile.

F Corresponding author. Email: stefania.biondi@unibo.it

Functional Plant Biology 38(10) 818-831 https://doi.org/10.1071/FP11088
Submitted: 12 April 2011  Accepted: 23 July 2011   Published: 16 September 2011

Abstract

Chenopodium quinoa Willd. (quinoa) is a halophyte for which some parameters linked to salt tolerance have been investigated separately in different genotypes and under different growth conditions. In this study, several morphological and metabolic responses were analysed in parallel after exposure to salinity. In vitro seed germination was initially delayed by a 150 mM NaCl treatment but eventually reached the same level as the control (0 mM NaCl), whereas seedling root growth was enhanced; both parameters were moderately inhibited (~35–50%) by 300 mM NaCl. In pot grown plants, plant size was reduced by increasing salinity (0–750 mM NaCl). Transpiration and stomatal conductance were decreased at the highest salinity levels tested, consistent with reduced stomatal density and size. The density of epidermal bladder cells (EBCs) on the leaf surface remained unaffected up to 600 mM NaCl. Tissue contents of Na+ and Cl increased dramatically with salt treatment, but resulted in only a 50% increase in Na+ from 150 to 750 mM NaCl. Internal K+ was unaffected up to 450 mM NaCl but increased at the highest salinity levels tested. Excretion through sequestration into EBCs was limited (generally ≤20%) for all ions. A modest dose-dependent proline accumulation, and concomitant reduction in total polyamines and putrescine efflux occurred in NaCl-treated plants. Results confirm the importance of inorganic ions for osmotic adjustment, the plant’s ability to maintain K+ levels and the involvement of putrescine efflux in maintaining ionic balance under high salinity conditions. Conversely, ion excretion and proline appear to play a minor role. Taken together these results indicate which parameters could be used for future comparison among different genotypes.

Additional keywords: ion homeostasis, osmoprotectant, salt glands.


References

Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.

Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138, 171–190.
Growth and development of Mesembryanthemum crystallinum (Aizoaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOhurs%3D&md5=6221e3569f6f19c5331f244b5e4f109eCAS |

Agarie S, Shimoda T, Shimizu Y, Baumann K, Sunagawa H, Kondo A, Ueno O, Nakahara T, Nose A, Cushman JC (2007) Salt tolerance, salt accumulation and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. Journal of Experimental Biology 58, 1957–1967.

Aguilar PC, Cutipa Z, Machaca E, Lopez M, Jacobsen SE (2003) Variation of proline content of quinoa (Chenopodium quinoa Willd.) in high beds (Waru Waru). Food Reviews International 19, 121–127.
Variation of proline content of quinoa (Chenopodium quinoa Willd.) in high beds (Waru Waru).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFyqt7Y%3D&md5=02fff00fcdda8ff1072d7f39bd43bdffCAS |

Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237–1249.
Polyamines: molecules with regulatory functions in plant abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Balestrini R, Galli L, Tartari G (2000) Wet and dry atmospheric deposition at prealpine and alpine sites in northern Italy. Atmospheric Environment 34, 1455–1470.
Wet and dry atmospheric deposition at prealpine and alpine sites in northern Italy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1ylurk%3D&md5=cb2423bd03be5162b9e503353e83f53bCAS |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline in water stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline in water stress studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=c827b48f99c0b89e93d36acb1c0f9680CAS |

Ben Hassine A, Ghanem ME, Bouzid S, Lutts S (2009) Abscisic acid has contrasting effects on salt excretion and polyamine concentrations of an inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus. Annals of Botany 104, 925–936.
Abscisic acid has contrasting effects on salt excretion and polyamine concentrations of an inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKisrjF&md5=05aa3210885b333950a2b093cad95893CAS |

Bosque-Sanchez H, Lemeur R, Van Damme P, Jacobsen SE (2003) Ecophysical analysis of drought and salinity stress of quinoa (Chenopodium quinoa Willd.). In ‘Quinoa – an Andean food group’. (Eds SE Jacobsen, A Mujica) pp. 111–119. (Marcel Dekker Inc.: New York)

Cataldi TRI, Margiotta G, Del Fiore A, Bufo SA (2003) Ionic content in plant extracts determined by ion chromatography with conductivity detection. Phytochemical Analysis 14, 176–183.
Ionic content in plant extracts determined by ion chromatography with conductivity detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOktbk%3D&md5=08a2e9e600bf6680019ad43c0db22365CAS |

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. Journal of Experimental Botany 58, 4245–4255.
Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymurg%3D&md5=e6e23648d109740fa7c2f9cf63a7cac3CAS |

Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl induced potassium efflux from barley root. Plant & Cell Physiology 46, 1924–1933.
Exogenously supplied compatible solutes rapidly ameliorate NaCl induced potassium efflux from barley root.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVOiug%3D%3D&md5=bf4b9060c5de73fb31d5c1d760a67377CAS |

Cuin TA, Shabala S (2007) Potassium efflux channels mediate Arabidopsis root responses to reactive oxygen species and the mitigating effect of compatible solutes. Plant, Cell & Environment 30, 875–885.
Potassium efflux channels mediate Arabidopsis root responses to reactive oxygen species and the mitigating effect of compatible solutes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFGiur4%3D&md5=daa1738cc70970e62a6e67068b2d5cbbCAS |

Das S, Bose A, Ghosh B (1995) Effect of salt stress on polyamine metabolism in Brassica campestris. Phytochemistry 39, 283–285.
Effect of salt stress on polyamine metabolism in Brassica campestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVCisbk%3D&md5=e8bada80585e63352efd7ece3e3e0ae3CAS |

Dasgan HY, Aktas H, Abak K, Cakmak I (2002) Determination of screening techniques to salinity tolerance in tomatoes and investigation of genotype responses. Plant Science 163, 695–703.
Determination of screening techniques to salinity tolerance in tomatoes and investigation of genotype responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVSgsr8%3D&md5=ef8e0e0933a51aa892109e2f5ba370fcCAS |

Delatorre-Herrera J, Pinto M (2009) Importance of ionic and osmotic components of salt stress on the germination of four Quinoa (Chenopodium quinoa Willd.) selections. Chilean Journal of Agricultural Research 69, 477–485.
Importance of ionic and osmotic components of salt stress on the germination of four Quinoa (Chenopodium quinoa Willd.) selections.Crossref | GoogleScholarGoogle Scholar |

Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123, 1468–1479.
Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1KmtL0%3D&md5=8e8c37dfb10091a6fbbebb7cae6fdef3CAS |

Dinelli G, Di Martino E, Vicari A (1998) Multi-determination of mineral ions in environmental water samples by capillary electrophoresis. Recent Research Developments in Agricultural and Food Chemistry 2, 435–442.

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=23566337824590a6cc47f8bef24d5a57CAS |

Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37, 604–612.
Evolution of halophytes: multiple origins of salt tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |

Freitas H, Breckle S-W (1993) Accumulation of nitrate in bladder hairs of Atriplex species. Plant Physiology and Biochemistry 31, 887–892.

Fuentes FF, Martinez EA, Hinrichsen PV, Jellen EN, Maughan PJ (2009) Assessment of genetic diversity patterns in Chilean quinoa (Chenopodium quinoa Willd.) germplasm using multiplex fluorescent microsatellite markers. Conservation Genetics 10, 369–377.
Assessment of genetic diversity patterns in Chilean quinoa (Chenopodium quinoa Willd.) germplasm using multiplex fluorescent microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFWhu7g%3D&md5=e4707481971c245b544b25a95b7d35a4CAS |

Hariadi Y, Marandon K, Tian Y, Jacobsen SE, Shabala S (2011) Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. Journal of Experimental Botany 62, 185–193.
Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurfM&md5=b02ec431c85e49327aaf1f0f10d337b7CAS |

Jacobsen SE, Mujica A, Jensen CR (2003) The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Reviews International 19, 99–109.
The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors.Crossref | GoogleScholarGoogle Scholar |

Janicka-Russak M, Kabala K, Miodzinska E, Klobus G (2010) The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. Journal of Plant Physiology 167, 261–269.
The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFOnsbg%3D&md5=02a59ac8de59818ee6f2f9c5c5f46eb2CAS |

Jensen CR, Jacobsen SE, Andersen MN, Núñez N, Andersen SD, Rasmussen L, Mogensen VO (2000) Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying. European Journal of Agronomy 13, 11–25.
Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying.Crossref | GoogleScholarGoogle Scholar |

Kavi Kishor PB, Sangam S, Amruth RN, Sri Laxmi P, Naidu KR, Rao KRSS, Sreenath Rao Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Current Science 88, 424–438.

Koyro HW, Eisa SS (2008) Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd. Plant and Soil 302, 79–90.
Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVGm&md5=887c7cb75c6ca5d84ab1a89d5154417bCAS |

Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228, 367–381.
Polyamines: essential factors for growth and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVCjsb8%3D&md5=227204e4c6c87c5eee5469be22d626c6CAS |

Lazarus BE, Richards JH, Gordon PE, Oki LR, Barnes CS (2011) Plasticity tradeoffs in salt tolerance mechanisms among desert Distichlis spicata genotypes. Functional Plant Biology 38, 187–198.
Plasticity tradeoffs in salt tolerance mechanisms among desert Distichlis spicata genotypes.Crossref | GoogleScholarGoogle Scholar |

Liphschitz N, Waisel Y (1982) Adaptation of plants to saline environments: salt excretion and glandular structure. In ‘Tasks for vegetation science’. (Eds DN Sen, KS Rajpurohit) pp. 197–214. (Dr W Junk Publishers: The Hague, The Netherlands)

Liu L, Shelp BJ (1996) Impact of chloride on nitrate absorption and accumulation by broccoli (Brassica oleracea var. italica). Canadian Journal of Plant Science 76, 367–377.
Impact of chloride on nitrate absorption and accumulation by broccoli (Brassica oleracea var. italica).Crossref | GoogleScholarGoogle Scholar |

Liu J-H, Inoue H, Moriguchi T (2008) Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots. Environmental and Experimental Botany 62, 28–35.
Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWqu77L&md5=ee0df761c5c7f6c677b933697d5c9a73CAS |

Lohaus G, Hussmann M, Pennewiss K, Schneider H, Zhu J-J, Sattelmacher B (2000) Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. Journal of Experimental Botany 51, 1721–1732.
Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVWis7o%3D&md5=b88fdcd41f023e79bc5c120d83dfc3a4CAS |

Luan S, Lan W, Chul Lee S (2009) Potassium nutrition, sodium toxicity and calcium signalling: connections through the CBL-CIPK network. Current Opinion in Plant Biology 12, 339–346.
Potassium nutrition, sodium toxicity and calcium signalling: connections through the CBL-CIPK network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFSjurk%3D&md5=5198f92d30bcbd7040f009c81ccb1d8cCAS |

Maggio A, Pascale SD, Ruggiero C, Barbieri G (2005) Physiological response of field grown cabbage to salinity and drought stress. European Journal of Agronomy 23, 57–67.
Physiological response of field grown cabbage to salinity and drought stress.Crossref | GoogleScholarGoogle Scholar |

Matysik J, Ali Bhalu B, Mohanty P (2002) Molecular mechanism of quenching of reactive oxygen species by proline under water stress in plants. Current Science 82, 525–532.

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=f51a15096130985e65701806a7266f1bCAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=4ff74227fb3898bf12208db44bd191acCAS |

Orsini F, D’Urzo MP, Inan G, Serra S, Oh DH, Mickelbart MV, Consiglio F, Li X, Jeong JC, Yun DJ, Bohnert HJ, Bressan RA, Maggio A (2010) A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana. Journal of Experimental Botany 61, 3787–3798.
A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7jO&md5=9b0f0ada6c334399b71505afd09b1cbeCAS |

Rosa M, Hilal M, Gonzalez JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiology and Biochemistry 47, 300–307.
Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVGrtLk%3D&md5=6d9e72578778b5d8b2e701b4ce195e5eCAS |

Ruffino AMC, Rosa M, Hilal M, Gonzalez JA, Prado FE (2010) The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity. Plant and Soil 326, 213–224.
The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrt7vN&md5=6d2f275a4d46dcd893e8df4e1234b3d7CAS |

Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency with special reference to the woodland flora. Philosophical Transactions of the Royal Society B 216, 848–852.

Santa-Cruz A, Perez-Alfocea F, Caro M, Acosta M (1998) Polyamines as short term salt tolerance traits in tomato. Plant Science 138, 9–16.
Polyamines as short term salt tolerance traits in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmt1ektLg%3D&md5=169b51721f2db99cb52ac9043f444836CAS |

Scaramagli S, Franceschetti M, Michael AJ, Torrigiani P, Bagni N (1999) Polyamines and flowering: spermidine biosynthesis in the different whorls of developing flowers of Nicotiana tabacum L. Plant Biosystems 133, 229–237.
Polyamines and flowering: spermidine biosynthesis in the different whorls of developing flowers of Nicotiana tabacum L.Crossref | GoogleScholarGoogle Scholar |

Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davis JM, Newman IA (2006) Extracellular calcium ameliorates NaCl induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ permeable channels. Plant Physiology 141, 1653–1665.
Extracellular calcium ameliorates NaCl induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ permeable channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitbo%3D&md5=8e2a4d7fb79da027e20b5d0ef4b8c905CAS |

Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1yit7s%3D&md5=3b58d0a7f0d410c4f355b83209f87bf2CAS |

Tamai T, Shimada Y, Sugimoto T, Shiraishi N, Oji Y (2000) Potassium stimulates the efflux of putrescine in roots of barley seedlings. Journal of Plant Physiology 157, 619–626.

Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45, 523–539.
Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislWit7w%3D&md5=239a1ba3f45c98fd8e0b5b4e0179f368CAS |

Wilson C, Read JJ, Abo-Kassem E (2002) Effect of mixed salt salinity on growth and ion relations of a quinoa and a wheat variety. Journal of Plant Nutrition 25, 2689–2704.
Effect of mixed salt salinity on growth and ion relations of a quinoa and a wheat variety.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsVOkt74%3D&md5=b7e626d2e6d9a5d28065d76a8146efbaCAS |