Selection of donors for salt-tolerance in tomato using physiological traits
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1 New Phytol. (1992), 121, Selection of donors for salt-tolerance in tomato using physiological traits J. CUARTERO\ A. R. YEO^ AND T. J. FLOWERS^ ^Estacion Experimental 'La Mayora', CSIC, 29750, Algarrobo Costa, Malaga, Spain 2 School of Biological Sciences, University of Sussex, Brighton, BNl 9QG, Sussex, UK {Received 7 August 1991; accepted 22 November 1991) SUMMARY Attempts to enhance the salt-tolerance of the cultivated tomato using the tolerance of related wild species of Lycopersicon Mill, have been unsuccessful commercially. An alternative approach is to attempt to accumulate physiological characters that contribute to tolerance within a genotype. We have investigated the relationships between tolerance and certain physiological characteristics in accessions of L. esculentum Mill., L. cheesmanii (Hook) C. H. Mull., L. pennellii (Correll) D'Arcy, L. peruvianum (L.) Mill, and L. pimpinellifolium Mill, with this aim in view. At a salinity equivalent to 40 % of that in an artificial seawater, the growth of young plants was ranked both in absolute terms (fresh weight, dry weight or the growth in area of a leaf that developed during the salt treatment) and relative to growth in a salinity 2 % of that of seawater. In absolute terms, two cultivars of L. esculentum ('Moneymaker' and 'Edkawy') performed about as well as L. pimpinellifolium and better than L. pennellii and L. cheesmanit : L. peruvtanum showed the poorest tolerance. In relative terms, L. pimpinellifolium remained the most tolerant of the species, and L. peruvianum the most sensitive, L, cheesmanii was little more tolerant than L. peruvianum. The five species differed in their succulence and the Na: K ratio in leaves that developed during the treatment with salinity. Succulence was higher at low salinity in L. pennellii and L, cheesmanii than in the other species, but increased less on salinization, L. pimpinellifolium showed the greatest increase in succulence on salinization, a consequence of its low water content in 2 % seawater. Sodium concentrations increased dramatically in all five species on salinization: L. pimpinellifolium had the highest and L. esculentum the lowest values. L. peruvianum was notable for maintaining a Na: K ratio of less than 3 throughout the period of the experiment. Key words: Breeding, physiological traits, salinity, tomato {Lycopersicon). [L. pennellii (Correll) D'Arcy and L. peruvianum (L.) INTRODUCTION j^.jj. ^^j^ ^g^^. p^inig g^ ^l, 1979; Tal & Shannon, The tomato is an important vegetable crop in semi- 1983], but in spite of the presence of these potential arid regions of Mediterranean countries. In these donors of tolerance and successful hybridizations, no regions soil and groundwater salinity are insidious cultivar suitable for commercial growers has been problems that affect agricultural productivity and developed so far. It appears that wide-crossing is increasing the tolerance of crop species such as not a simple solution. Rather, it may be necessary tomato to salinity is an aim of contemporary plant to discover the individual physiological processes breeding. One approach to this goal is to attempt to that confer tolerance and accumulate these within a transfer genetic information from a related salt- genotype (Yeo & Flowers, 1989). Thus, the main tolerant species. In the case of cultivated tomato, objective of the work reported here was to determine Lycopersicon esculentum Mill., an accession (LA whether there were physiological traits that differed 1401) of the wild relative L. cheesmanii (Hook) C. H. between Lycopersicon accessions that might be useful Mull was identified as salt-tolerant by Rush & in a future breeding programme. Epstein (1976) and used in breeding programmes L. pennellii, L. peruvianum, and L. cheesmanii, are with the cultivated tomato (Rush & Epstein, 1981 a). not genetically very close to L. esculentum and the L. cheesmanii is ecologically a halophyte, having been transfer of genetic information between these species observed to grow close to the sea in the Galapagos is not an easy task. An accession (PE-2) of L. Islands. There are also other species within the genus pimpinellifolium Mill., which has been shown to be Lycopersicon, which have been identified as tolerant relatively salt-tolerant (Cruz & Cuartero, 1987), has
2 64 y. Cuartero, A. R. Yeo and T.J. Elowers a particular value in that it is readily crossed with L. esculentum and has been used as a donor of other useful characters (Stevens & Rick, 1986). Our second objective was therefore to compare the tolerance of L. pimpinellifolium with that of reputedly tolerant species to ascertain which would be the better for use as a donor for salt-tolerance traits. MATERIALS AND METHODS The accessions used were L. esculentum cv. ' Moneymaker', an established European commercial cultivar, L. esculentum cv. 'Edkawy', an Egyptian cultivar with a reputation for salinity resistance, and the species reported as tolerant: L. pimpinellifolium, L. peruvianum and L. pennellii (accessions PE-2, PE- 22 and PE-47, respectively, collected in Peru by Cuartero, Nuez & Diaz 1984) and L. cheesmanii (accession LA-1401 from Dr F. Nuez, Valencia Polytechnic University, Spain). Seeds were germinated in Petri dishes on filter paper and then transplanted into blocks (8 cm'*) of ' Rockwool' and placed on a 100 mm layer of gravel. The Rockwool had little influence on the plants as they grew since most of the roots were in the gravel. Nutrient solution was pumped into the trays to flood them to the surface of the ' Rockwool' for 5 min every 3 h; gravity drained the system over the next 5 min. The nutrient solution was a modified Hoagland solution containing artificial seawater (ASW; see Flowers et al., 1990) to provide \o\\- and highsalt treatments. These were equivalent to either 2 or 40% seawater: that is to 9 or 183 mol m =* Na (21 and 21 ds m^'), respectively. The concentrations of the major nutrients were (mol m^^): K, 3 ; NH^, 0-5 ; Mg, 1; Ca, 2-5; NO,,, 3; H^PO,, 0-5; SO,, 1; Cl, 5. Fifty-six plants of each genotype were grown from February to April in a glasshouse. Treatments were applied when the plants had between 4 and 6 true leaves. Minimum temperatures were C and daily maxima were C. Supplementary lighting was provided for 12 h per day at 200 //mol m^^ s"' PAR and maximum light levels were 800//mol m"^ s^'. Just prior to the time that salt treatments were applied, the youngest expanding leaf, about 10 mm in length, was tagged for identification at later harvests. Eight plants of each species or cultivar were harvested the day before the salinization began (designated harvest / = 0) and subsequently a further eight plants were harvested for each of the treatments (2 and 40 "o ASW) at 6, 12 and 34 d after salinization. Shoot fresh weight was recorded. The area of the tagged leaf was measured with an Area Quantifier (Model 528, KGM Vidiaids Ltd). Harvested material was dried at 60 C for at least 48 h and the dry weights recorded. Succulence was calculated as the water content per unit leaf area. Dried tagged-leaves were extracted in acetic acid (100 mol m^^) at 90 C for 2 h for analysis; Na and K were determined in the extract by atomic absorption spectrophotometry and Cl with an ion-selective electrode. RESULTS Plant growth Growth was used to characterize the overall tolerance of plants to salinity - both in absolute and relative terms. All the lines increased in weight both in 2 and 40% ASW (Fig. 1) over the 35 d of the experiment. There were, however, clear differences among the accessions in absolute growth at low salinity (2 % ASW), and in relative growth reduction between 2 and 40 % ASW (Fig. 2). At low salinity, the cultivars of L. esculentum produced more dry weight than any of the other accessions, although both L. pennellii (PE-47) and L. cheesmanii (LA 1401) were similar to ' Edkawy' in terms of fresh weight. Rankings of the six lines tested were similar whether based on fresh or dry weight or the area of the tagged leaf ('Moneymaker' > 'Edkawy' ^ L. cheesmanii > L. pennellii > L. pimpinellifolium > L. peruvianum). At the higher salinity (40 o ASW), the best and worst 100 T (a) ^ 0 '5 03 o x: C/ Time (days) Figure 1. The increase in fresh weight of the shoot of six Lycopersicon accessions with time when grown in either (a) 2"o or (b) 40% artificial seawater. The accessions and the symbols used to represent them are: Lycopersicon esculentum cv. ' Moneymaker' (A), L. esculentum cv. ' Edkawy' ( ), L. pimpinellifolium (T), L. peruvianum ( ), L. pennellii {^) and L. cheesmanii (#).
3 Donors for salt tolerance in tomato 65 CD en a> on all three counts (fresh and dry weight and leaf area), while L. peruvianum remained the poorest (Fig. 2). The overall rankings based on all three measures of growth were: L. pimpinellifolium > 'Edkawy' > L. pennellii > 'Moneymaker' * L. cheesmanii > L. peruvianum. Relative dry matter production of L. pimpinellifolium at 40 " ASW' was more than half that in 2 o ASW, considerably better than any other accession tested B 7-5 'o % 50 > D J E o are +.- ra LSD P = I I 13 [x LSC P = OC Money-Edkawy L. L. L. L. maker pitnp. peruv. penn. chees. Figure 2. The growth, expressed in terms of fresh weight, dry weight and leaf area of six accessions of Lycopersicon in 2% (D) and 40 o ( ) artificial seawater (ASW), The numerals show the growth in 40 % ASW relative to that in 2 o ASW, The abbreviations used are: Moneymaker- Lycopersicon esculentum cv, 'Moneymaker'; Edkawy-7>, esculentum cv,'edkawy'; L, pimp. - L. pimpinellifolium (PE-2); L, peruv. - L. peruvianum (PE-22); L. penn. - L, pennellii (PE-47) and L. chees. - L. cheesmanii (LA1401), lines remained the same, with some change in the middle order so that averaging the three criteria, the rankings were: 'Moneymaker' > 'Edkawy' ^ L. pimpinellifolium > L. pennellii ^ L. cheesmanii > L. peruvianum. The pattern changed, however, if the lines were ranked in terms of growth at 40 "o ASW relative to that at 2"o ASW. For this relativegrowth, it did not matter whether fresh weight or leaf area, were used as the ranking criterion, although there was a little variation when dry weight was used as the basis (mainly due to L. cheesmanii). L. pimpinellifolium was the most salt tolerant accession Water content and succulence In low salinity, water content per unit dry weight of leaf tissue, varied considerably between accessions: L. pennellii and L. cheesmanii had higher water contents than the other species (Table 1). At high salinity water content tended to increase with time (data not shown), though these differences were significant only by the final harvest (34 d after salinization) when water contents were more similar between accessions than at low salinity, although those of L. esculentum were lower than those of the other species. The two species with high water contents at low salinity (L. pennellii and L. cheesmanii) showed a much smaller increase in water content than the other species, L. esculentum, L. pimpinellifolium and L. peruviantim. The water content of leaf tissue can also be expressed in terms of the leaf area ~- an index often termed succulence and one that is not influenced by changes in the dry weight per unit area. In L. esculentum and Z^. cheesmanii there was a more pronounced increase in succulence with leaf age than occurred with the other species; but this was not affected by salinity (data not shown). All the accessions increased their succulence when grown at the higher salinity: the increase was, however, very much greater for L. pimpinellifolium than for the other species - a consequence of the low succulence of this species at low salinity. Ion concentrations and contents Because of changes in water content with treatment and time ion contents are best expressed taking the water content of the tissue into consideration. Leaf Na concentrations in plants treated with 2"o ASW were very similar at the three harvests, ranging from a mean of 14-5 mol m"'' after 6 d to 11-8 after 34 d. The lowest mean value for the three harvests was 9-0 mol m''' for L. esculentum cv. 'Edkawy' and the highest 20-7 mol m~^ for L. pimpinellifolium (PE-2). The sodium concentration increased dramatically in all five species following salinization to 40 "o ASW - by an average of just over four-fold in comparison with the concentrations prior to salinization over a period of 6 d (Table 2). The concentrations then fell somewhat over the next 6 d in all but L. pimpinellifolium, rising again over the next 22 d. The,\N1' 121
4 66 J. Cuartero, A. R. Yeo and T.J. Flowers Table 1. The water content {g water per g dry weight) and succulence (g water per unit leaf area) of six accessions of Lycopersicon. The data are for what was the youngest expanded leaf at the time of salinization of plants that were grown in either 2% or 40% artificial seawater (ASW) for 34 d. Accession Moneymaker Edkawy L. pimp. L. peruv. L. penn. L. chees. 2 % ASW 40 % ASW "o change (40%/2%) 2 ".-o ASW 40% ASW % change (40%/2%) 5-6 ± ± ± Water content (g g"^ dry 5-0 ± ±O Succulence (g m"^ 324 ± ± ± f-68 weight) 6-0 ± ± ± ± ± ± ± Abbreviations used: Moneymaker - Lycopersicon esculentum cv. ' Moneymaker'; Edkawy - L. esculentum cv. 'Edkawy'; L. pimp. - L. pimpinellifolium (PE-2); L. peruv. - L. peruvianum (PE-22); L. penn. - L. pennellii (PE-47) and L. chees. - L. cheesmanii (LA1401). Table 2. The concentration of potassium and sodium {mol m~^ of plant water) in what was the youngest expanded leaf at the time of salinization of six accessions of Lycopersicon. The data are for plants that were grown in 40% artificial seawater {ASW) Time from salinization with 40 % ASW Accession Sodium Moneymaker* Edkawy L. pimp. L. peruv. L. penn. L. chees. Mean Potassium Moneymaker Edkawy L. pimp. L. peruv. L. penn L. chees. Mean 24±10 23± ± ±17 29±5 291 ±9 297 ± ± ± ±9 107±12 80 ±24 151± ± ±20 121±14 133± ± ±27 125±14 60± ± ± ± ± ± ± ± ±31 40±ll ±17 39±34 26 ±6 41 ±7 * Abbreviations as in Table 1. decline in salt concentrations between 6 and 12 d after salinization may represent a period of adjustment between growth and ion accumulation: the data in Table 2 all refer to a leaf that was growing rapidly at the time of salinization. By the time of the final harvest, L. pimpinellifolium (PF-2) showed the highest leaf Na concentration followed by L. pennellii (PF-47): the concentrations in the accessions, L. cheesmanii (LA 1401) and L. peruvianum (PF-22) were similar. The lowest concentrations were in L. esculentum 'Moneymaker' and 'Edkawy' (Table 2). There were small, but significant, differences in the potassium concentrations within the tagged leaves at the initial (f = 0) harvest: L. peruvianum had the highest and L. cheesmanii the lowest potassium concentrations. In the low salinity treatment, the potassium concentration in the tagged leaf declined in all the species, from an average of 302 ±9 mol m~* plant water at t 0, to 115 ± 5 mol m~^ by day 6 and then to 71 ± 9 mol m^^ by the final harvest at day 34. There was no notable difference between the accessions. Following salinization of the plants with 40 % ASW, the potassium concentrations again decreased with time in all of the species. Sodium did not increase the rate of decline in potassium concentration over the first 12 d, except in L. pimpinellifolium, although by day 34 the average potassium concentration was only 65 ± 19 % of that
5 .. ^ ^ ^ Donors for salt tolerance in tomato k 6 Z Youngest expanded at time = yv I 1 1 / L. pimp leaf / p L penn. - / 1 1 L Time from salinization (days) y" L Chees. D Edkawy.,,.- Mmaker" * L peruv. Figure 3. The change in sodium to potassium ratio with time in what was the youngest expanded leaf (tagged leaf, see Materials and Methods) at the time of salinization in six accessions of Lycopersicon grown in 40% artificial seawater. The abbreviations used are: Mmaker - Lycopersicon esculentum cv. ' Moneymaker'; Edkawy-L. esculentum cv. 'Edkawy'; L. pimp.-l. pimpinellifolium (PE-2); L. peruv.-l. peruvianum (PE-22); L. penn. - L. pennellii (PE-47) and L. chees.-l. cheesmanii (LAI401). from the equivalent tagged leaf of plants grown in 2 % ASW. L. peruvianum was exceptional in retaining an higher potassium concentration in 40% than in 2 % ASW (146 % of the 2 % ASW value). If the data for L. peruvianum are excluded from the 34 d averages, then the other accessions had just under 50 % of the potassium concentration of the plants grown in 2 % ASW - to be contrasted with the 146 % in L. peruvianum. So, by the final harvest, the lowest potassium concentrations were recorded in L. cheesmanii and L. pimpinellifolium while the highest was in L. peruvianum (Table 2). The average concentration of sodium plus potassium prior to the salinization of the plants (the harvest at t = 0) was similar in all the accessions ( mol m~^). At the lower salinity this value declined sharply, over the first 6 d to mol m-^ and finally to 82±11 mol m"'' after 34 d. At the higher salinity, which represented an increase in the external sodium concentration of 174 mol m"^, (Na+K) concentrations in the leaf tissue were higher than the external concentration at the final harvest by an average of about 80 mol m"^ (Table 2): L. pimpinellifolium, L. peruvianum and L. pennellii all maintained differences greater than the increase in the external concentration. The Na:K ratio, calculated from the leaf sodium and potassium concentrations, showed a similar trend for all the species except L. peruvianum (PE- 22). In the latter, the Na: K ratio remained less than three throughout the period of the experiment (Fig. 3), while the ratio rose in all the other species. The maximum values were recorded for L. pimpinellifolium, the species that showed the greatest tolerance to salt as judged by the growth parameters. However, there was no overall correlation between growth I under saline conditions and the Na:K ratio. Shannon, Gronwald & Tal (1987) also failed to find any relationship between Na: K ratio and tolerance in a range of tomato species. DISCUSSION There is considerable variability in the reported tolerances of various species of Lycopersicon to sodium chloride. While some measurements of growth under saline relative to non-saline conditions have suggested that L. cheesmanii was more tolerant than L. esculentum (Rush & Epstein, 1976; Tal & Shannon, 1983), other experiments have shown this not always to be the case (Shannon et al., 1987). In our experiments both L. esculentum 'Moneymaker' and 'Edkawy' were more tolerant than L. cheesmanii LA Similar discrepancies can be found in reported measurements of the relative tolerance of other species. Thus while L. peruvianum has been reported more tolerant than L. pennellii (Tal & Shannon, 1983; Shannon et al., 1987) this is not always so (Phillis et al, 1979; Fig. 2). This all suggests that there is considerable variation between accessions within species. If growth alone were the most important criterion in the tolerance of salinity, ' Moneymaker' would be the line of choice. However, yields of this cultivar were reduced more than those of L. pimpinellifolium (PE-2) by high salinity. On the other hand, although PE-2 has a substantial degree of salt tolerance, it lacks the vigour of the commercial L. esculentum cultivars in the absence of salinity and its fruit are too small to be of commercial value. Consequently, introducing the tolerance of L. pimpinellifolium to L. esculentum is a reasonable goal and feasible because of the closeness between the two species: genes from PE-2, mainly with resistance to diseases, have been incorporated into L. esculentum on previous occasions (Stevens & Rick, 1986). There are three practical considerations. The first is the need to understand tolerance in L. pimpinellifolium and whether possible effects on yield potential are acceptable. The second is how to recognize salt tolerance traits efficiently during a breeding programme. Selection will have to be focussed upon the tolerance traits, while allowing undesirable features of the L. pimpinellifolium genome to be deleted. To answer this and the previous question necessitates a knowledge of the physiological basis of salt-tolerance in L. pimpinellifolium. Finally, the nature of the inheritance of any traits important in tolerance must eventually be determined in order to design the most appropriate breeding programme. Two physiological traits that varied between species were immediately obvious from our experiments - succulence and Na: K ratio. The development of succulence in response to salinity is a common observation in dicotyledonous 5-2
6 68 J. Cuartero, A. R. Yeo and T. J. Elowers halophytes (Flowers, Hajibagheri & Clipson, 1986). Such an increase in the water content of a plant might mitigate against excessive ion concentrations. Tal et al. (1979) and Tal & Shannon (1983) reported succulence as a fresh weight: dry weight ratio before and after NaCl treatment of a number of accessions of wild and cultivated tomato. They (Tal & Shannon, 1983) found that increases in this ratio were greater in L. pennellii than in L. esculentum, L. cheesmanii or L. peruvianum. Surprisingly, they did not find salinity increased the ratio of fresh to dry weight in L. esculentum. However, since the ratio of fresh to dry weight changed with time and the accessions were different from those we have used, it is not possible to make simple comparisons. Increasing succulence with increasing leaf chloride concentration has been reported in another member of the Solanaceae, tobacco (Flowers, Flowers & Greenway, 1986). Such increases in succulence with increasing ion concentration may be indicative of successful storage of ions within the vacuoles. In contrast, a decline in the water content has been correlated with extracellular dehydration brought about by ions present in the cell walls (Oertli, 1968; Flowers et al, 1991). Overall, neither succulence nor increase in succulence were clearly correlated with the response of growth, although L. pimpinellifolium does show, on salinization, the maximal increase in succulence and the minimal relative reduction in growth of any of the species tested. If the increase in succulence reflects the compartmentalization of solutes it would be a valuable trait to transfer to L. esculentum. Cultivars of L. esculentum have been reported to have low sodium ion concentrations relative to other genera of Lycopersicon, when grown under saline conditions (Tal, 1971 ; Rush & Epstein, 1976; Tal et al, 1979; Phillis et al, 1979; Tal & Shannon, 1983), although ion concentrations have generally been reported on the basis of the dry weight. In our experiments, the two cultivars of L. esculentum had lower sodium ion concentrations in the tagged leaf expressed on a dry weight basis than the other species (data not shown) and the ranking of accessions remained essentially the same when calculated on the water-based concentrations. Ion concentrations do, however, depend on the state of the plants and can rise dramatically if they succumb to the external salinity (e.g. Rush & Epstein, 1976): there was no indication, however, that this stage had been reached in our experiments (Fig. 1). Although the ability to maintain potassium uptake in the presence of high concentrations of external sodium may be a desirable trait, there is no reason why this should have been selected for during evolution in species that are not halophytes. If such characters vary independently of overall tolerance, as suggested by Yeo & Flowers (1989), L. peruvianum (PE-22) might be a valuable donor of this trait in spite of its overall poor performance under saline conditions. However, the data for the tagged leaf are confounded with the ability to mobilize potassium as the leaf ages. Consequently, the value of the Na:K ratio in the youngest (expanding) leaf of the plant should be a better overall indicator of the ability of the plant to select and utilize potassium under sodium salinization. The relationship between growth and ion concentrations in the shoot has been investigated on a number of occasions (Tal, 1971; Rush & Epstein, 1976; Rush & Epstein, 1981b; Sacher, Staples & Robinson, 1983; Tal & Shannon, 1983; Shannon et al, 1987), although only Sacher et al. (1983) have used regression analysis to compare growth with ion concentrations - within cultivars of L. esculentum. They found a significant relationship between the dry weight of plants under saline conditions, expressed relative to the control plants, and the leaf ion accumulation, again expressed relative to control plants, such that growth declined as ion accumulation increased. Between the accessions evaluated here the dry weight of the shoots under saline conditions (relative to the control plants) was related to the ion concentration in the tagged leaf at the final harvest, namely dry weight (%) = x ion concentration (mol m^'*); the regression accounted for 57% of the variance. Such relationships between growth and ion concentrations have been reported for other species (see Greenway & Munns, 1980 for a review) although there is no a priori reason why they should account for the greater part of the variance (see Yeo et al, 1990 for a full discussion). We conclude that succulence and good selectivity for potassium over sodium are important to salttolerance in tomato. These traits are clearly recognizable, might be transferred to L. esculentum during a breeding programme and there is no reason why they should not be compatible with the high yield required of a commercial cultivar. L. pimpinellifolium (PE-2) was the species showing the best salttolerance. This species is genetically the closest to L. esculentum in the genus which makes L. pimpinellifolium a good candidate, to be included in breeding programmes for salt-tolerance. ACKNOWLEDGEMENTS We would like to thank Sam Flowers for her help with some of the experiments, the Royal Society for a European Fellowship (to J.C), the CICYT for partial support of this research (Project AGR89-O536) and the British Council for a travel grant (to T.J.F.), REFERENCES CRIZ, V, & CUARTERO, J, (1987), Growth and fruiting of the tomato and related species in saline conditions. In: Modern Trends in Tomato Genetics and Breeding (Ed, by S, Porcelli, L, M, Monti & M, Cirulli), pp, , Research Institute for Vegetable Crops, Pontecagnano, Salerno, Italy, CUARTERO, J,, NUEZ, F, & DIAZ, A, (1984), Catalog of collections
7 Donors for salt tolerance in tomato 69 oi Lycopersicon and S. pennellii from Northwest of Peru. Report of the Tomato Genetics Cooperative 34, FLOWERS, T. J., FLOWERS, S. A. & GREENWAY, H. (1986). Effects of sodium chloride on tohacco plants. Plant, Cell and Environment 9, FLOWERS, T. J., FLOWERS, S. A., HAJIBAGHERI, M. A., & YEO, A. R. (1990). Salt tolerance in the halophytic wild rice Porfresia coarctata Tateoka. New Phytologist 114, FLOWERS, T. J., FLOWERS, S. A., HAJIBAGHERI, M. A. & YEO, A. R. (1991). Ion accumulation in the cell walls of rice plants growing under saline conditions: evidence for the Oertli hypothesis. Plant, Cell and Environment 14, FLOWERS, T. J., HAJIBAGHERI, M. A., & CLIPSON, N. J. W. (1986). HALOPHYTES. Quarterly Review of Biology 61, GREENWAY, H. & MUNNS, R. (1980). Mechanisms of salt tolerance in nonhalophytes. Annual Review of Plant Physiology OERTLI, J. J. (1968). Extracellular salt accumulation, a possihle mechanism of salt injury in plants. Agrochimica 12, PHILLIS, B. R., PECK, N. H., MACDONALD, G. E. & ROBINSON, R. W. (1979). Differential response oi Lycopersicon and Solanum species to salinity. Journal of the American Society for Horticultural Science 104, RUSH, D. W. & EPSTEIN, E. (1976). Genotypic responses to salinity. Differences hetween salt-sensitive and salt-tolerant genotypes of the tomato. Plant Physiology 57, RUSH, D. W. & EPSTEIN, E. (1981a). Breeding and selection for salt tolerance hy the incorporation of wild germplasm into a domestic tomato. Journal of the American Society for Horticultural Science 106, RUSH, D. W. & EPSTEIN, E. (19816). Comparative studies on the sodium potassium and chloride relations of a wild halophytic and a domestic salt sensitive tomato species. Plant Physiology 68, SACHER, R. F., STAPLES, R. C. & ROBINSON, R. W. (1983). Ion regulation and response of tomato to sodium chloride a homeostatic system. Journal of the American Society for Horticultural Science 108, SHANNON, M. C, GRONWALD, J. W. & TAL, M. (1987). Effects of salinity on growth and accumulation of organic and inorganic ions in cultivated and wild tomato species. Journal of the American Society for Horticultural Science 112, STEVENS, M. A. & RICK, C. M. (1986). Genetics and breeding. In: The Tomato Crop (Ed. by J. G. Atherton & J. Rudich), pp Chapman and Hall, London. TAL, M. (1971). Salt tolerance in the wild relatives of the cultivated tomato responses of Lycopersicon esculentum, L. peruvianum and L. esculentum minor to sodium chloride solution. Australian Journal of Agricultural Research 22, TAL, M., K\TZ, A., HEIKIN, H. & DEHAN, K. (1979). Salt tolerance in the wild relatives of the cultivated tomato. Proline accumulation in Lycopersicon esculentum Mill, L. peruvianum Mill and Solanum pennellii Cor., treated with NaCl and polyethylene glycol. Neiv Phytologist 82, TAL, M. & SHANNON, M. C. (1983). Sah tolerance in the wild relatives of the cultivated tomato. Responses of Lycopersicon esculentum, L. cheesmanii, L. peruvianum, Solanum pennellii and Fj hybrids to high salinity. Australian Journal of Plant Physiology 10, YEO, A. R. & FLOWERS, T. J. (1989). Selections for physiological characters examples from breeding for salt resistance. In: Plants under Stress (Ed. by H. G. Jones, T. J. Flowers & M. B. Jones), pp Cambridge University Press, Cambridge. YEO, A. R., YEO, M. E., FLOWERS, S. A. & FLOWERS, T. J. (1990). Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance and their relationship to overall performance. Theoretical and Applied Genetics 79,
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