Seawater stress applied at germination affects mitochondrial function in durum wheat (Triticum durum) early seedlings
Zina Flagella A B D , Daniela Trono A C , Marianna Pompa A , Natale Di Fonzo C and Donato Pastore A BA Dipartimento di Scienze Agroambientali, Chimica e Difesa Vegetale, Università di Foggia, Via Napoli, 25-71100 Foggia, Italy.
B Centro di Ricerea Interdipartimentale BIOAGROMED, Università di Foggia, Via Napoli, 6/B-71100 Foggia, Italy.
C Istituto Sperimentale per la Cerealicoltura C.R.A., SS 16 Km 675-71100 Foggia, Italy.
D Corresponding author. Email: z.flagella@unifg.it
Functional Plant Biology 33(4) 357-366 https://doi.org/10.1071/FP05244
Submitted: 4 October 2005 Accepted: 2 February 2006 Published: 3 April 2006
Abstract
Seawater stress effects on mitochondrial ATP synthesis and membrane potential (ΔΨ) were investigated in germinating durum wheat seedlings under moderate (22% seawater osmolarity, –0.62 MPa) and severe (37% seawater osmolarity, –1.04 MPa) stress. To estimate the osmotic component of salt stress, mannitol solutions (0.25 and 0.42 m) iso-osmotic with the saline ones were used. Moderate stress intensity only delayed mean germination time (MGT), whereas higher seawater osmolarity reduced germination percentage as well. In contrast, Na+ and Cl– accumulation showed a sharp increase under moderate stress and only a small further increase under severe stress, which was more pronounced for Cl–. Only severe stress significantly damaged succinate-dependent oxidative phosphorylation, which may be related to the stress-induced alteration in inner mitochondrial membrane permeability, as indicated by changes in ΔΨ profiles. Proline-dependent oxidative phosphorylation, however, was inhibited under moderate stress. This suggests the occurrence of an adaptation mechanism leading to proline accumulation as an osmoprotectant. Moreover, both the osmotic and the toxic components of seawater stress were detrimental to oxidative phosphorylation. Damage to germination and MGT, in contrast, were mainly caused by osmotic stress. Therefore, mitochondrial function appears to be a more sensitive target of toxic stress than growth. In conclusion, the effects of seawater stress on mitochondrial ATP synthesis vary in relation to the substrate oxidised and stress level, inducing both adaptive responses and damage.
Keywords: durum wheat, mitochondrial ATP synthesis, plant mitochondria, osmotic stress, salt stress, seawater.
Acknowledgments
This work was supported by grants from the University of Foggia to Z Flagella, under the project ‘Physiological indicators of salt tolerance in durum wheat’. We thank Dr Lucia Vittozzi who participated as a student in this work.
Åkerman EOK, Wikström KFM
(1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Letters 68, 191–197.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alia P, Pardha Saradhi P
(1993) Suppression in mitochondrial electron transport is the prime cause behind stress induced proline accumulation. Biochemical and Biophysical Research Communications 193, 54–58.
| Crossref |
PubMed |
Almansouri M,
Kinet J-M, Lutts S
(2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant and Soil 231, 243–254.
| Crossref | GoogleScholarGoogle Scholar |
Bates LS,
Waldren RP, Teare ID
(1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
| Crossref |
Caliandro A, Cucci G, De Caro A, Cordella S
(1991) Irrigation with brackish water: influence of the irrigation regime on salt built-up in the soil and leaching effect of rainfall. In ‘Proceedings of the European Mediterranean conference on the use of saline water in irrigation, Valenzeno (BA)’. (IAMB: Italy)
Carillo P,
Mastrolonardo G,
Nacca F, Fuggi A
(2005) Nitrate reductase in durum wheat seedlings as affected by nitrate nutrition and salinity. Functional Plant Biology 32, 209–219.
| Crossref | GoogleScholarGoogle Scholar |
Casolo V,
Braidot E,
Chiandussi E,
Vianello A, Macrì F
(2003) K+ATP channel opening prevents succinate-dependent H2O2 generation by plant mitochondria. Physiologia Plantarum 118, 313–318.
| Crossref | GoogleScholarGoogle Scholar |
Delauney AJ, Verma DPS
(1993) Proline biosynthesis and osmoregulation in plants. The Plant Journal 4, 215–223.
| Crossref | GoogleScholarGoogle Scholar |
Dizengremel P
(1983) Effect of Triton X-100 on electron transport in plant mitochondria. Physiologie Vegetale 21, 731–741.
Douce R,
Bourguignon J,
Brouquisse R, Neuburger M
(1987) Isolation of plant mitochondria: general principles and criteria of integrity. Methods in Enzymology 148, 403–415.
Dutilleul C,
Garmier M,
Noctor G,
Mathieu C,
Chétrit P,
Foyer CH, de Paepe R
(2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signalling and diurnal regulation. The Plant Cell 15, 1212–1226.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Elia A,
Santamaria P, Serio F
(1996) Ammonium and nitrate influence on artichoke growth rate and uptake of inorganic ions. Journal of Plant Nutrition 19, 1029–1044.
Ellis RH, Ellis RH
(1980) Towards a rational basis for testing seed quality. In ‘Seed production’. (Ed. PD Hebblethwaite)
pp. 605–635. (Butterworths: London)
Flagella Z,
Cantore V,
Giuliani MM,
Tarantino E, De Caro A
(2002) Crop salt tolerance: physiological, yield and quality aspects. Recent Research Development in Plant Biology 2, 155–186.
Francois LE, Maas EV
(1994) Crop response and management of salt-affected soils. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakli)
pp. 149–181. (Marcel Dekker Inc.: New York)
Fratianni A,
Pastore D,
Pallotta ML,
Chiatante D, Passarella S
(2001) Increase of membrane permeability of mitochondria isolated from water stress adapted potato cells. Bioscience Reports 21, 81–91.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goldstein AH,
Anderson JO, McDaniel RG
(1980) Cyanide-insensitive and cyanide-sensitive O2 uptake in wheat. Plant Physiology 66, 488–493.
Gomez JM,
Hernandez JA,
Jimenez A,
del Rio LA, Sevilla F
(1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radical Research 31, 8–15.
Greenway H, Munns R
(1980) Mechanisms of salt tolerance in nonhalophytes. Plant Physiology 31, 149–190.
| Crossref | GoogleScholarGoogle Scholar |
Hamilton EW, Heckathorn SA
(2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas Complex II is protected by proline and betaine. Plant Physiology 126, 1266–1274.
| Crossref | GoogleScholarGoogle Scholar |
Harris DA
(1987) Spectrophotometric assays. In ‘Spectrophotometry & spectrofluorimetry: a practical approach’. (Eds CL Bashford, DA Harris)
pp. 59–61. (IRL Press: Oxford)
Hasegawa PM,
Bressan RA,
Zhu JK, Bohnert HJ
(2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology 51, 463–499.
| Crossref | GoogleScholarGoogle Scholar |
Hu Y,
Fricke W, Schmidhalter U
(2005) Salinity and the growth of non-halophytic grass leaves: the role of mineral nutrient distribution. Functional Plant Biology 32, 973–985.
| Crossref | GoogleScholarGoogle Scholar |
Husain S,
Munns R, Condon AG
(2003) Effect of sodium exclusion trait on chlorophyll retention and growth of durum wheat in saline soil. Australian Journal of Agricultural Research 54, 589–597.
| Crossref | GoogleScholarGoogle Scholar |
Husain S,
von Caemmerer S, Munns R
(2004) Control of salt transport from roots to shoots of wheat in saline soil. Functional Plant Biology 31, 1115–1126.
| Crossref | GoogleScholarGoogle Scholar |
Jolivet Y,
Pireaux JC, Dizengremel P
(1990) Changes in properties of barley leaf mitochondria isolated from NaCl-treated plants. Plant Physiology 94, 641–646.
Kasai K,
Mori N, Nakamura C
(1998) Changes in the respiratory pathways during germination and early seedling growth of common wheat under normal and NaCl-stressed conditions. Cereal Research Communications 26, 217–224.
Katerji N,
van Hoorn JW,
Hamdy A, Mastrorilli M
(2000) Salt tolerance classification of crops according to soil salinity and to water stress day index. Agricultural Water Management 43, 99–109.
| Crossref | GoogleScholarGoogle Scholar |
Kingsbury RW, Epstein E
(1986) Salt sensitivity in wheat. Plant Physiology 80, 651–654.
Klein RR,
Burke JJ, Wilson RF
(1986) Effect of osmotic stress on ion transport processes and phospholipid composition of wheat (Triticum aestivum L.) mitochondria. Plant Physiology 82, 936–941.
Kromer S, Heldt HW
(1991) Respiration of pea leaf mitochondria and redox transfer between the mitochondrial and the extra-mitochondrial compartment. Biochimica et Biophysica Acta 1057, 42–50.
Kuiper PJC
(1980) Lipid metabolism of higher plants in saline environments. Physiologie Vegetale 18, 83–88.
Lindsay MP,
Lagudah ES,
Hare RA, Munns R
(2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Functional Plant Biology 31, 1105–1114.
| Crossref | GoogleScholarGoogle Scholar |
Livne A, Levin N
(1967) Tissue respiration and mitochondrial oxidative phosphorylation of NaCl-treated pea seedlings. Plant Physiology 42, 407–414.
Logan DC,
Millar AH,
Sweetlove LJ,
Hill SA, Leaver CJ
(2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiology 125, 662–672.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lutts S,
Almansouri M, Kinet J-M
(2004) Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus. Plant Science 167, 9–18.
| Crossref | GoogleScholarGoogle Scholar |
McKersie, B ,
and
Leshem, YY (Eds) (1994).
Moore AL, Proudlove MO
(1987) Purification of plant mitochondria on silica sol gradients. Methods in Enzymology 148, 415–420.
Munns R
(2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Muranaka S,
Shimizu K, Kato M
(2002) Ionic and osmotic effects of salinity on single-leaf photosynthesis in two wheat cultivars with different drought tolerance. Photosynthetica 40, 201–207.
| Crossref | GoogleScholarGoogle Scholar |
Pasternak D, De Malach Y
(1994) Crop irrigation with saline water. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakli)
pp. 599–622. (Marcel Dekker Inc.: New York)
Pastore D,
Greco M,
Petragallo VA, Passarella S
(1994) Increase in H+ / e– ratio of the cytochrome c oxidase reaction in mitochondria irradiated with helium–neon laser. Biochemistry and Molecular Biology International 34, 817–826.
| PubMed |
Pastore D,
Stoppelli MC,
Di Fonzo N, Passarella S
(1999a) The existence of the K+ channel in plant mitochondria. Journal of Biological Chemistry 274, 26683–26690.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pastore D,
Trono D, Passarella S
(1999b) Substrate oxidation and ADP / ATP exchange in coupled durum wheat (Triticum durum Desf.) mitochondria. Plant Biosystems 133, 219–228.
Pastore D,
Fratianni A,
Di Pede S, Passarella S
(2000) Effects of fatty acids, nucleotides and reactive oxygen species on durum wheat mitochondria. FEBS Letters 470, 88–92.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pastore D,
Trono D,
Laus MN,
Di Fonzo N, Passerella S
(2001) Alternative oxidase in durum wheat mitochondria. Activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant & Cell Physiology 42, 1373–1382.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pastore D,
Laus MN,
Di Fonzo N, Passarella S
(2002) Reactive oxygen species inhibit the succinate oxidation-supported generation of membrane potential in wheat mitochondria. FEBS Letters 516, 15–19.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peckmann K, Herppich WB
(1998) Effects of short-term drought and rewatering on the activity of mitochondrial enzymes and the oxidative capacity of leaf mitochondria from a CAM plant: Aptenia cordifolia. Journal of Plant Physiology 152, 518–524.
Petit PX
(1992) Flow cytometric analysis of rhodamine 123 fluorescence during modulation of the membrane potential in plant mitochondria. Plant Physiology 98, 279–286.
Petrussa E,
Casolo V,
Peresson C,
Braidot E,
Vianello A, Macrì F
(2004) The K+ATP channel is involved in a low-amplitude permeability transition in plant mitochondria. Mitochondrion 3, 297–307.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rana G, Katerji N
(2000) Measurement and estimation of actual evapotranspiration in the field under Mediterranean climate: a review. European Journal of Agronomy 13, 125–153.
| Crossref | GoogleScholarGoogle Scholar |
Rivelli AR,
James RA,
Munns R, Condon AG
(2002) Effect of salinity on water relations and growth of wheat genotypes with contrasting sodium uptake. Functional Plant Biology 29, 1065–1074.
| Crossref | GoogleScholarGoogle Scholar |
Schmitt N, Dizengremel P
(1989) Effect of osmotic stress on mitochondria isolated from etiolated mung bean and sorghum seedlings. Plant Physiology and Biochemistry 27, 17–26.
Schwarz M,
Henri RL, Reinhold L
(1991) Mitochondria isolated from NaCl-adapted tobacco cell lines (Nicotiana tabacum / gossii) maintain their phosphorylative capacity in highly saline media. Plant Physiology 96, 69–76.
Sells GD, Koeppe DE
(1981) Oxidation of proline by mitochondria isolated from water-stressed maize shoots. Plant Physiology 68, 1058–1063.
Stewart CR,
Boggess SF,
Aspinall D, Paleg LG
(1977) Inhibition of proline oxidation by water stress. Plant Physiology 59, 930–932.
Sweetlove LJ,
Heazlewood JL,
Herald V,
Holtzapffel R,
Day DA,
Leaver CJ, Millar AH
(2002) The impact of oxidative stress on Arabidopsis mitochondria. The Plant Journal 32, 891–904.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taylor CB
(1996) Proline and water deficit: ups, downs, ins, and outs. The Plant Cell 8, 1221–1223.
| Crossref | GoogleScholarGoogle Scholar |
Tezara W,
Mitchell VJ,
Driscoll SD, Lawlor DW
(1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 40, 914–917.
Thomas JS,
Sepahi M,
Arendall B, Bohnert HJ
(1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant, Cell & Environment 18, 801–806.
Trono D,
Flagella Z,
Laus MN,
Di Fonzo N, Pastore D
(2004) The uncoupling protein and the potassium channel are activated by hyperosmotic stress in mitochondria from durum wheat seedlings. Plant, Cell & Environment 27, 437–448.
| Crossref | GoogleScholarGoogle Scholar |
Voetberg GS, Sharp RE
(1991) Growth of maize primary root at low water potential. III. Role of increased proline deposition in osmotic adjustment. Plant Physiology 96, 1125–1130.
Whitehouse DG,
Fricaud AC, Moore AL
(1989) Role of nonohmicity in the regulation of electron transport in plant mitochondria. Plant Physiology 91, 487–492.
Zhu JK
(2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zottini N,
Mandolino G, Zannoni D
(1993) Oxidation of external NAD(P)H by mitochondria from taproots and tissue cultures of sugar beet (Beta vulgaris). Plant Physiology 102, 579–585.
| PubMed |