Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effects of abiotic stresses on sorbitol biosynthesis and metabolism in tomato (Solanum lycopersicum)

Afaf Almaghamsi A , Marta Nosarzewski A , Yoshinori Kanayama B and Douglas D. Archbold https://orcid.org/0000-0002-6471-5836 A C
+ Author Affiliations
- Author Affiliations

A University of Kentucky, Department of Horticulture, N318 Agricultural Science Centre 7 North, Lexington, KY 40546, USA.

B Graduate School of Agricultural Science, Tohoku University, 468-1 Aramaki Aza-Aoba, Aoba-ku, Sendai 980-8572, Japan.

C Corresponding author. Email: darchbol@uky.edu

Functional Plant Biology - https://doi.org/10.1071/FP20065
Submitted: 12 March 2020  Accepted: 29 September 2020   Published online: 26 October 2020

Abstract

Polyols such as sorbitol and ribitol are a class of compatible solutes in plants that may play roles in tolerance to abiotic stresses. This study investigated the effects of water stress on sorbitol biosynthesis and metabolism and sorbitol and ribitol accumulation in tomato (Solanum lycopersicum L.). Water stress induced by withholding water and by using polyethylene glycol as a root incubation solution to mimic water stress, and NaCl stress were applied to wild-type (WT) and three genetically-modified lines of tomato (cv. Ailsa Craig), a control vector line TR22, and 2 sorbitol dehydrogenase (sdh) antisense lines TR45 and TR49. Sorbitol and ribitol content, as well as the enzymatic activities, protein accumulation, and gene expression patterns of the key sorbitol cycle enzymes aldose-6-phosphate reductase (A6PR), aldose reductase (AR), and sorbitol dehydrogenase (SDH), were measured in mature leaves. In response to the stresses, both sorbitol and ribitol accumulated in leaf tissue, most significantly in the sdh antisense lines. A6PR, characterised for the first time in this work, and AR both exhibited increased enzymatic activity correlated with sorbitol accumulation during the stress treatments, with SDH also increasing in WT and TR22 to metabolise sorbitol, reducing the content to control levels within 3 days after re-watering. In the sdh antisense lines, the lack of significant SDH activity resulted in the increased sorbitol and ribitol content above WT levels. The results highlighted a role for both A6PR and AR in biosynthesis of sorbitol in tomato where the high activity of both enzymes was associated with sorbitol accumulation. Although both A6PR and AR are aldo-keto reductases and use NADPH as a co-factor, the AR-specific inhibitor sorbinil inhibited AR only indicating that they are different enzymes. The determination that sorbitol, and perhaps ribitol as well, plays a role in abiotic responses in tomato provides a cornerstone for future studies examining how they impact tomato tolerance to abiotic stresses, and if their alteration could improve stress tolerance.

Keywords: abiotic stress, aldose reductase, aldose-6-phosphate reductase, drought stress, polyol, salt stress, Solanum lycopersicum, sorbitol dehydrogenase, sugar alcohols, tomato.


References

Aguayo MF, Cáceres JC, Fuentealba M, Muñoz R, Stange C, Cabrera R, Handford M (2015) Polyol specificity of recombinant Arabidopsis thaliana sorbitol dehydrogenase studied by enzyme kinetics and in silico modeling. Frontiers in Plant Science 6, 91
Polyol specificity of recombinant Arabidopsis thaliana sorbitol dehydrogenase studied by enzyme kinetics and in silico modeling.Crossref | GoogleScholarGoogle Scholar | 25755662PubMed |

Bohren KM, Grimshaw CE (2000) The sorbinil trap: a predicted dead-end complex confirms the mechanism of aldose reductase inhibition. Biochemistry 39, 9967–9974.
The sorbinil trap: a predicted dead-end complex confirms the mechanism of aldose reductase inhibition.Crossref | GoogleScholarGoogle Scholar | 10933817PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

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 | 18182428PubMed |

Conde A, Regalado A, Rodrigues D, Costa JM, Blumwald E, Chaves MM, Gerós H (2015) Polyols in grape berry: transport and metabolic adjustments as a physiological strategy for water-deficit stress tolerance in grapevine. Journal of Experimental Botany 66, 889–906.
Polyols in grape berry: transport and metabolic adjustments as a physiological strategy for water-deficit stress tolerance in grapevine.Crossref | GoogleScholarGoogle Scholar | 25433029PubMed |

de Sousa SM, Paniago MG, Arruda P, Yunes JA (2008) Sugar levels modulate sorbitol dehydrogenase expression in maize. Plant Molecular Biology 68, 203–213.
Sugar levels modulate sorbitol dehydrogenase expression in maize.Crossref | GoogleScholarGoogle Scholar | 18566893PubMed |

Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biology 8, 131
Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process.Crossref | GoogleScholarGoogle Scholar | 19102748PubMed |

Flörke M, Schneider C, McDonald RI (2018) Water competition between cities and agriculture driven by climate change and urban growth. Nature Sustainability 1, 51–58.
Water competition between cities and agriculture driven by climate change and urban growth.Crossref | GoogleScholarGoogle Scholar |

Food and Agriculture Organization (2017) FAOSTAT database. Available http://faostat3.fao.org/ [Verified 30 September 2020]

Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 20870416PubMed |

Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou D, Giovannonni J, Kanellis AK (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. Journal of Experimental Botany 60, 663–678.
Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions.Crossref | GoogleScholarGoogle Scholar | 19129160PubMed |

Kanayama Y, Sakanishi K, Mori H, Yamaki S (1995) Expression of the gene encoding NADP-dependent sorbitol-6-phosphate dehydrogenase in apple seedlings. Plant & Cell Physiology 36, 1139–1141.
Expression of the gene encoding NADP-dependent sorbitol-6-phosphate dehydrogenase in apple seedlings.Crossref | GoogleScholarGoogle Scholar |

Königshofer H (1983) Changes in ion composition and hexitol content of different Plantago species under the influence of salt stress. Plant and Soil 72, 289–296.
Changes in ion composition and hexitol content of different Plantago species under the influence of salt stress.Crossref | GoogleScholarGoogle Scholar |

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 5432063PubMed |

Lee SP, Chen THH (1993) Expression of an aldose reductase‐related gene during the induction of freezing‐tolerance in bromegrass cell suspension cultures. Journal of Plant Physiology 142, 749–753.
Expression of an aldose reductase‐related gene during the induction of freezing‐tolerance in bromegrass cell suspension cultures.Crossref | GoogleScholarGoogle Scholar |

Lo Bianco R, Rieger M, Sung SJS (2000) Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach. Physiologia Plantarum 108, 71–78.
Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach.Crossref | GoogleScholarGoogle Scholar |

Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiologia Plantarum 70, 553–557.
Physiology and metabolism of sugar alcohols in higher plants.Crossref | GoogleScholarGoogle Scholar |

Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth management practices to prevent and mitigate soil salinization. Horticulturae 3, 30
Soil salinity: effect on vegetable crop growth management practices to prevent and mitigate soil salinization.Crossref | GoogleScholarGoogle Scholar |

Mehta RA, Parsons BL, Mehta AM, Nakhasi HL, Mattoo AK (1991) Differential protein metabolism and gene expression in tomato fruit during wounding stress. Plant & Cell Physiology 32, 1057–1065.
Differential protein metabolism and gene expression in tomato fruit during wounding stress.Crossref | GoogleScholarGoogle Scholar |

Nangare DD, Singh Y, Kumar PS, Minhas PS (2016) Growth, fruit yield and quality of tomato (Lycopersicon esculentum Mill.) as affected by deficit irrigation regulated on phenological basis. Agricultural Water Management 171, 73–79.
Growth, fruit yield and quality of tomato (Lycopersicon esculentum Mill.) as affected by deficit irrigation regulated on phenological basis.Crossref | GoogleScholarGoogle Scholar |

Negm FB (1986) Purification and properties of an NADPH-aldose reductase (aldehyde reductase) from Euonymus japonica leaves. Plant Physiology 80, 972–977.
Purification and properties of an NADPH-aldose reductase (aldehyde reductase) from Euonymus japonica leaves.Crossref | GoogleScholarGoogle Scholar | 16664750PubMed |

Nosarszewski M, Clements AM, Downie AB, Archbold DD (2004) Sorbitol dehydrogenase expression and activity during apple fruit set and early development. Physiologia Plantarum 121, 391–398.
Sorbitol dehydrogenase expression and activity during apple fruit set and early development.Crossref | GoogleScholarGoogle Scholar |

Nosarszewski M, Downie AB, Wu B, Archbold DD (2012) The role of sorbitol dehydrogenase in Arabidopsis thaliana. Functional Plant Biology 39, 462–470.
The role of sorbitol dehydrogenase in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Ohta K, Moriguchi R, Kanahama K, Yamaki S, Kanayama Y (2005) Molecular evidence of sorbitol dehydrogenase in tomato, a non-Rosaceae plant. Phytochemistry 66, 2822–2828.
Molecular evidence of sorbitol dehydrogenase in tomato, a non-Rosaceae plant.Crossref | GoogleScholarGoogle Scholar | 16289145PubMed |

Ranney TG, Bassuk NL, Whitlow TH (1991) Osmotic adjustment and solute constituents in leaves and roots of water-stressed cherry (Prunus) trees. Journal of the American Society for Horticultural Science 116, 684–688.
Osmotic adjustment and solute constituents in leaves and roots of water-stressed cherry (Prunus) trees.Crossref | GoogleScholarGoogle Scholar |

Richardson JS, Carpena X, Switalta J, Perez-Luque R, Donald LJ, Loewen PC, Oresnik IJ (2008) RhaU of Rhizobium leguminosarum is a rhamnose mutarotase. Journal of Bacteriology 190, 2903–2910.
RhaU of Rhizobium leguminosarum is a rhamnose mutarotase.Crossref | GoogleScholarGoogle Scholar | 18156270PubMed |

Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell & Environment 25, 163–171.
The role of glycine betaine in the protection of plants from stress: clues from transgenic plants.Crossref | GoogleScholarGoogle Scholar |

Sengupta D, Reddy AR, Naik D (2015) Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: a structure-function update. Journal of Plant Physiology 179, 40–55.
Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: a structure-function update.Crossref | GoogleScholarGoogle Scholar | 25840343PubMed |

Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057–1060.
Hydroxyl radical scavenging activity of compatible solutes.Crossref | GoogleScholarGoogle Scholar |

Song XM, Yu Q, Dong X, Yang HO, Zeng KW, Li J, Tu PF (2017) Aldose reductase inhibitors attenuate β-amyloid-induced TNF-α production in micrologia via ROS-PKC-mediated NF-κB and MAPK pathways. International Immunopharmacology 50, 30–37.
Aldose reductase inhibitors attenuate β-amyloid-induced TNF-α production in micrologia via ROS-PKC-mediated NF-κB and MAPK pathways.Crossref | GoogleScholarGoogle Scholar | 28623716PubMed |

Sree BK, Rajendrakumar CSV, Reddy AR (2000) Aldose reductase in rice (Oryza sativa L): stress response and developmental specificity. Plant Science 160, 149–157.
Aldose reductase in rice (Oryza sativa L): stress response and developmental specificity.Crossref | GoogleScholarGoogle Scholar |

Stoop JMH, Williamson JD, Pharr DM (1996) Mannitol metabolism in plants: a method for coping with stress. Trends in Plant Science 1, 139–144.
Mannitol metabolism in plants: a method for coping with stress.Crossref | GoogleScholarGoogle Scholar |

Suekawa M, Fujikawa Y, Inada S, Murano A, Esaka M (2016) Gene expression and promoter analysis of a novel tomato aldo-keto reductase in response to environmental stresses. Journal of Plant Physiology 200, 35–44.
Gene expression and promoter analysis of a novel tomato aldo-keto reductase in response to environmental stresses.Crossref | GoogleScholarGoogle Scholar | 27337067PubMed |

Sutsawat D, Yamada K, Shiratake K, Kanayama Y (2008) Properties of sorbitol dehydrogenase in strawberry fruit and enhancement of the activity by fructose and auxin. Journal of the Japanese Society for Horticultural Science 77, 318–323.
Properties of sorbitol dehydrogenase in strawberry fruit and enhancement of the activity by fructose and auxin.Crossref | GoogleScholarGoogle Scholar |

Tari I, Kiss G, Deér AK, Csiszár J, Erdei L, Gallé Á, Gémes K, Horváth F, Poór P, Szepesi Á, Simon LM (2010) Salicylic acid increased aldose reductase activity and sorbitol accumulation in tomato plants under salt stress. Biologia Plantarum 54, 677–683.
Salicylic acid increased aldose reductase activity and sorbitol accumulation in tomato plants under salt stress.Crossref | GoogleScholarGoogle Scholar |

Wang Z, Stutte GW (1992) The role of carbohydrates in active osmotic adjustment in apple under water stress. Journal of the American Society for Horticultural Science 117, 816–823.
The role of carbohydrates in active osmotic adjustment in apple under water stress.Crossref | GoogleScholarGoogle Scholar |

Williamson J, Jennings D, Ehrenshaft M, Guo WW, Pharr DM (2002) Sugar alcohols, salt stress, and fungal resistance: Polyols – multifunctional plant protection. Journal of the American Society for Horticultural Science 127, 467–473.
Sugar alcohols, salt stress, and fungal resistance: Polyols – multifunctional plant protection.Crossref | GoogleScholarGoogle Scholar |

Zhou R, Cheng L, Wayne R (2003) Purification and characterization of sorbitol-6-phosphate phosphatase from apple leaves. Plant Science 165, 227–232.
Purification and characterization of sorbitol-6-phosphate phosphatase from apple leaves.Crossref | GoogleScholarGoogle Scholar |