Salinization of water and soil has a negative impact on tomato (Solanum lycopersicum L.) productivity by reducing growth of sink organs and by inducing senescence in source leaves. It has been hypothesized that yield stability implies the maintenance or increase of sink activity in the reproductive structures, thus contributing to the transport of assimilates from the source leaves through changes in sucrolytic enzymes and their regulation by phytohormones. In this study, classical and functional physiological approaches have been integrated to study the influence of metabolic and hormonal factors on tomato fruit sink activity, growth, and yield: (i) exogenous hormones were applied to plants, and (ii) transgenic plants overexpressing the cell wall invertase (cwInv) gene CIN1 in the fruits and de novo cytokinin (CK) biosynthesis gene IPT in the roots were constructed. Although salinity reduces fruit growth, sink activity, and trans-zeatin (tZ) concentrations, it increases the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) during the actively growing period (25 days after anthesis). Indeed, exogenous application of the CK analogue kinetin to salinized actively growing fruits recovered sucrolytic activities (mainly cwInv and sucrose synthase), sink strength, and fruit weight, whereas the ethylene-releasing compound ethephon had a negative effect in equivalent non-stressed fruits. Fruit yield was increased by both the constitutive expression of CIN1 in the fruits (up to 4-fold) or IPT in the root (up to 30%), owing to an increase in the fruit number (lower flower abortion) and in fruit weight. This is possibly related to a recovery of sink activity in reproductive tissues due to both (i) increase in sucrolytic activities (cwInv, sucrose synthase, and vacuolar and cytoplasmic invertases) and tZ concentration, and (ii) a decrease in the ACC levels and the activity of the invertase inhibitor. This study provides new functional evidences about the role of metabolic and hormonal inter-regulation of local sink processes in controlling tomato fruit sink activity, growth, and yield under salinity.

Department of Plant Nutrition CEBAS CSIC Campus de Espinardo 30100 Murcia Spain

Department of Plant Nutrition CEBAS CSIC Campus de Espinardo 30100 Murcia Spain Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria

Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria Department of Plant and Environmental Sciences Copenhagen Plant Science Centre University of Copenhagen Højbakkegård Allé 13 DK 2630 Taastrup Denmark

Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria Department of Plant and Environmental Sciences Copenhagen Plant Science Centre University of Copenhagen Højbakkegård Allé 13 DK 2630 Taastrup Denmark Global Change Research Centre Czech Globe AS CR v v i Drásov 470 Cz 664 24 Drásov Czech Republic

Instituto de Bioquímica Vegetal y Fotosíntesis Universidad de Sevilla CSIC 41092 Sevilla Spain

Molecular Plant Pathology Laboratory USDA ARS Beltsville MD 20705 USA

Zobrazit více v PubMed

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. Journal of Experimental Botany 59, 4119–4131 PubMed PMC

Albacete A, Grosskinsky DK, Roitsch T. 2011. Trick and treat: A review on the function and regulation of plant invertases in the abiotic stress response. Phyton - Annales Rei Botanicae 50, 181–204

Albacete A, Martínez-Andújar C, Ghanem ME, Acosta M, Sánchez-Bravo J, Asins MJ, Cuartero J, Lutts S, Dodd IC, Pérez-Alfocea F. 2009. 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 and Environment 32, 928–938 PubMed

Albacete AA, Martínez-Andújar C, Pérez-Alfocea F. 2014. Hormonal and metabolic regulation of source–sink relations under salinity and drought: From plant survival to crop yield stability. Biotechnology Advances 32, 12–30 PubMed

Ariizumi T, Shinozaki Y, Ezura H. 2013. Genes that influence yield in tomato. Breeding Science 63, 3–13 PubMed PMC

Baldet P, Hernould M, Laporte F, Mounet F, Just D, Mouras A, Chevalier C, Rothan C. 2006. The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants. Journal of Experimental Botany 57, 961–970 PubMed

Balibrea ME, Cuartero J, Bolarín MC, Pérez-Alfocea F. 2003. Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity. Physiologia Plantarum 118, 38–46 PubMed

Balibrea ME, Dell’Amico J, Bolarín MC, Pérez-Alfocea F. 2000. Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiologia Plantarum 110, 503–511

Balibrea ME, Martínez-Andújar C, Cuartero J, Bolarín MC, Pérez-Alfocea F. 2006. The high fruit soluble sugar content in wild Lycopersicon species and their hybrids with cultivars depends on sucrose import during ripening rather than on sucrose metabolism. Functional Plant Biology 33, 279–288 PubMed

Balibrea ME, Parra M, Bolarín MC, Pérez-Alfocea F. 1999. Cytoplasmic sucrolytic activity controls tomato fruit growth under salinity. Australian Journal of Plant Physiology 26, 561–568

Balibrea ME, Santa Cruz AM, Bolarín MC, Pérez-Alfocea F. 1996. Sucrolytic activities in relation to sink strength and carbohydrate composition in tomato fruit growing under salinity. Plant Science 118, 47–55

Baxter CJ, Carrari F, Bauke A, Overy S, Hill SA, Quick PW, Fernie AR, Sweetlove LJ. 2005. Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant and Cell Physiology 46, 425–437 PubMed

Beck EH. 1996. Regulation of shoot/root ratio by cytokinins from roots in Urtica dioica: Opinion. Plant and Soil 185, 3–12

Ben Salah I, Albacete A, Martínez Andújar C, Haouala R, Labidi N, Zribi F, Martinez V, Pérez-Alfocea F, Abdelly C. 2009. Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress. Journal of Plant Physiology 166, 477–488 PubMed

Bertin N, Buret M, Gary C. 2001. Insights into the formation of tomato quality during fruit development. The Journal of Horticultural Sciences and Biotechnology 76, 786–792

Bohner J, Bangerth F. 1988. Effects of fruit set sequence and defoliation on cell number, cell size and hormone levels of tomato fruits (Lycopersicon esculentum Mill.) within a truss. Plant Growth Regulation 7, 141–155

Bonfig KB, Gabler A, Simon UK, Luschin-Ebengreuth N, Hatz M, Berger S, Muhammad N, Zeier J, Sinha AK, Roitsch T. 2010. Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Molecular Plant 3, 1037–1048 PubMed

Cara B, Giovannoni JJ. 2008. Molecular biology of ethylene during tomato fruit development and maturation. Plant Science 175, 106–113

Cramer GR. 1992. Kinetics of maize leaf elongation: II. Responses of a Na-excluding cultivar and a Na-including cultivar to varying Na/Ca salinities. Journal of Experimental Botany 43, 857–864

Cuartero J, Fernández-Muñoz R. 1998. Tomato and salinity. Scientia Horticulturae 78, 83–125

Chazen O, Hartung W, Neumann PM. 1995. The different effects of PEG 6000 and NaCl on leaf development are associated with differential inhibition of root water transport. Plant, Cell and Environment 18, 727–735

Daie J. 1996. Metabolic adjustments, assimilate partitioning, and alterations in source-sink relations in drought-stressed plants. In: Zamski E, Schaffer AA, eds. Photoassimilate distribution in plants and crops: source-sink relationships. New York: Marcel Dekker, Inc., 407–420

Damon S, Hewitt J, Nieder M, Bennett AB. 1988. Sink metabolism in tomato fruit: II. Phloem unloading and sugar uptake. Plant Physiology 87, 731–736 PubMed PMC

De Jong M, Mariani C, Vriezen WH. 2009. The role of auxin and gibberellin in tomato fruit set. Journal of Experimental Botany 60, 1523–1532 PubMed

Ehness R, Roitsch T. 1997. Coordinated induction of extracellular invertase and glucose transporters in Chenopodium rubrum by cytokinins. Plant Journal 11, 539–548 PubMed

Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE. 1993. Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Molecular Biology 21, 515–524 PubMed

Eschrich W. 1980. Free space invertase, its possible role in phloem unloading. Berichte der Deutschen Botanischen Gesellschaft 93, 363–378

Fridman E, Carrari F, Liu Y-S, Fernie AR, Zamir D. 2004. Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305, 1786–1789 PubMed

Garrido G, Ramón Guerrero J, Angel Cano E, Acosta M, Sánchez-Bravo J. 2002. Origin and basipetal transport of the IAA responsible for rooting of carnation cuttings. Physiologia Plantarum 114, 303–312 PubMed

Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F. 2008. Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). Journal of Experimental Botany 59, 3039–3050 PubMed PMC

Ghanem ME, Albacete A, Smigocki AC, et al. 2011. Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. Journal of Experimental Botany 62, 125–140 PubMed PMC

Ghanem ME, Van Elteren J, Albacete A, Quinet M, Martínez-Andújar C, Kinet JM, Pérez-Alfocea F, Lutts S. 2009. Impact of salinity on early reproductive physiology of tomato (Solanum lycopersicum) in relation to a heterogeneous distribution of toxic ions in flower organs. Functional Plant Biology 36, 125–136 PubMed

Gillaspy G, Ben-David H, Gruissem W. 1993. Fruits: A developmental perspective. The Plant Cell Online 5, 1439–1451 PubMed PMC

Godt DE, Roitsch T. 1997. Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiology 115, 273–282 PubMed PMC

Großkinsky DK, Naseem M, Abdelmohsen UR, et al. 2011. Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiology 157, 815–830 PubMed PMC

Guivarc’h A, Rembur J, Goetz M, Roitsch T, Noin M, Schmülling T, Chriqui D. 2002. Local expression of the ipt gene in transgenic tobacco (Nicotiana tabacum L. cv. SR1) axillary buds establishes a role for cytokinins in tuberization and sink formation. Journal of Experimental Botany 53, 621–629 PubMed

Hartig K, Beck E. 2006. Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biology 8, 389–396 PubMed

Ho LC. 1984. Partitioning of assimilates in fruiting tomato plants. Plant Growth Regulation 2, 277–285

Ho LC. 1996. The mechanism of assimilate partitioning and carbohydrate compartmentation in fruit in relation to the quality and yield of tomato. Journal of Experimental Botany 47, 1239–1243 PubMed

Ho LC, Grange RI, Shaw AF. 1989. Source/sink regulation. In: Baker DA, Milburn JA, eds. Transport and Photoassimilates. Essex: Longman Scientific and Technical, 306–343

Hocking PJ, Steer BT. 1994. The distribution and identity of assimilates in tomato with special reference to stem reserves. Annals of Botany 73, 315–325

Hsiao TC. 1973. Plant responses to water stress. Annual Review of Plant Physiology 24, 519–570

Jin Y, Ni DA, Ruan YL. 2009. Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21, 2072–2089 PubMed PMC

Klann EM, Chetelat RT, Bennett AB. 1993. Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiology 103, 863–870 PubMed PMC

Koch K. 2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235–246 PubMed

Kuiper D. 1993. Sink strength: Established and regulated by plant growth regulators. Plant, Cell and Environment 16, 1025–1026

Lara MEB, Garcia MCG, Fatima T, Ehness R, Lee TK, Proels R, Tanner W, Roitsch T. 2004. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16, 1276–1287 PubMed PMC

Linden JC, Ehneß R, Roitsch T. 1996. Ethylene regulation of apoplastic invertase expression in autotrophic cells of Chenopodium rubrum . Plant Growth Regulation 19, 219–222

Marcelis L. 1996. Sink strength as a determinant of dry matter partitioning in the whole plant. Journal of Experimental Botany 47, 1281. PubMed

Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N. 2011. Fruit-set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents. Journal of Plant Growth Regulation 30, 405–415

Matsuo S, Kikuchi K, Fukuda M, Honda I, Imanishi S. 2012. Roles and regulation of cytokinins in tomato fruit development. Journal of Experimental Botany 63, 5569–5579 PubMed PMC

Mayak S, Borochov A. 1984. Nonosmotic inhibition by sugars of the ethylene-forming activity associated with microsomal membranes from carnation petals. Plant Physiology 76, 191–195 PubMed PMC

McCurdy DW, Dibley S, Cahyanegara R, Martin A, Patrick JW. 2010. Functional characterization and RNAi-mediated suppression reveals roles for hexose transporters in sugar accumulation by tomato fruit. Molecular Plant 3, 1049–1063 PubMed

Mothes K, Engelbrecht L, Schütte H. 1961. Uber die akkumulation von a-aminoisobuttersa ure im blattgewebe unter dem einfluss von kinetin. Physiologia Plantarum 14, 72–75

Munns R. 1993. Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell and Environment 16, 15–24

Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239–250 PubMed

Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681 PubMed

Pérez-Alfocea F, Albacete A, Ghanem ME, Dodd IC. 2010. Hormonal regulation of source-sink relations to maintain crop productivity under salinity: A case study of root-to-shoot signalling in tomato. Functional Plant Biology 37, 592–603

Roitsch T. 1999. Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 2, 198–206 PubMed

Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK. 2003. Extracellular invertase: Key metabolic enzyme and PR protein. Journal of Experimental Botany 54, 513–524 PubMed

Roitsch T, Ehness R. 2000. Regulation of source/sink relations by cytokinins. Plant Growth Regulation 32, 359–367

Roitsch T, Ehness R, Goetz M, Hause B, Hofmann M, Sinha AK. 2000. Regulation and function of extracellular invertase from higher plants in relation to assimilate partitioning, stress responses and sugar signalling. Functional Plant Biology 27, 815–825

Roitsch T, González MC. 2004. Function and regulation of plant invertases: Sweet sensations. Trends in Plant Science 9, 606–613 PubMed

Ruan Y-L, Patrick J. 1995. The cellular pathway of postphloem sugar transport in developing tomato fruit. Planta 196, 434–444

Sakakibara H. 2006. Cytokinins: Activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431–449 PubMed

Santa-Cruz A, Martinez-Rodriguez MM, Perez-Alfocea F, Romero-Aranda R, Bolarin MC. 2002. The rootstock effect on the tomato salinity response depends on the shoot genotype. Plant Science 162, 825–831

Serrani JC, Ruiz-Rivero O, Fos M, García-Martínez JL. 2008. Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant Journal 56, 922–934 PubMed

Srivastava A, Handa A. 2005. Hormonal regulation of tomato fruit development: A molecular perspective. Journal of Plant Growth Regulation 24, 67–82

Stearns JC, Glick BR. 2003. Transgenic plants with altered ethylene biosynthesis or perception. Biotechnology Advances 21, 193–210 PubMed

Sturm A. 1999. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiology 121, 1–7 PubMed PMC

Swartzberg D, Dai N, Gan S, Amasino R, Granot D. 2006. Effects of cytokinin production under two SAG promoters on senescence and development of tomato plants. Plant Biology 8, 579–586 PubMed

Van der Werf A, Nagel OW. 1996. Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose: Opinion. Plant and Soil 185, 21–32

Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C. 2008. Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytologist 177, 60–76 PubMed

Warren-Wilson J. 1972. Control of crop processes. In: Rees AR, ed. Crop processes in controlled environments. Sussex: Academic Press Inc, 7–30

Yin Y-G, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C. 2010. Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ‘Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner. Journal of Experimental Botany 61, 563–574 PubMed PMC

Zanor MI, Osorio S, Nunes-Nesi A, et al. 2009. RNA interference of LIN5 in tomato confirms its role in controlling brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology 150, 1204–1218 PubMed PMC

Bacillus licheniformis FMCH001 Increases Water Use Efficiency via Growth Stimulation in Both Normal and Drought Conditions

Metabolic Control of Tobacco Pollination by Sugars and Invertases

The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions

Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato