Source: UNIVERSITY OF KENTUCKY submitted to
DEFINING THE ROLE(S) OF PLANT SORBITOL DEHYDROGENASE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
NEW
Funding Source
Reporting Frequency
Annual
Accession No.
1002522
Grant No.
(N/A)
Project No.
KY011040
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Feb 3, 2014
Project End Date
Sep 30, 2018
Grant Year
(N/A)
Project Director
Archbold, D.
Recipient Organization
UNIVERSITY OF KENTUCKY
500 S LIMESTONE 109 KINKEAD HALL
LEXINGTON,KY 40526-0001
Performing Department
Horticulture
Non Technical Summary
Sorbitol metabolism plays important roles in key events in many plant species. In apple, the most important temperate zone tree fruit in the world, all aspects of fruit development and quality are dependent on the main product of photosynthesis - sorbitol - and its accumulation by fruit. Inefficient utilization of sorbitol at the key step of conversion of sorbitol to fructose by SORBITOL DEHYDROGENASE (SDH) in the fruit can adversely affect the fruit. Knowledge of apple SDH response to the environment and to horticultural practices could lead to improvements in yield and fruit quality.SDH also appears to play a novel role in stress tolerance in many species for which sorbitol is only a minor compound, including the model plant species Arabidopsis thaliana. We discovered that SDH also plays a key role in metabolism of ribitol that seems directly related to drought stress. Improving abiotic stress tolerance of crop species is critical in the face of the anticipated long-term effects of climate change. Seasonal temperatures, rainfall patterns, etc., are expected to change in ways challenging to crop production, while the global human population is expected to increase substantially. Thus, crop yields will need to increase, by some estimates up to 70% more than present levels, under more adverse conditions. All avenues of crop plant improvement will need to be exploited by plant breeding and by genetic engineering to keep pace, and new avenues, exemplified by the direction of the proposed work, will need to be developed to the fullest. The basic knowledge gained by studying the role of SDH in metabolism of sorbitol and ribitol in Arabidopsis could lead to new horticultural and/or biochemical/genetic strategies to optimize plant abiotic stress tolerance in crop plant species.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
0%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2061110100025%
2061110104025%
2062420100025%
2062420104025%
Goals / Objectives
The long term goal of the project is to understand the role(s), and the factors regulating expression and activity, of SORBITOL DEHYDROGENASE (SDH) in apple and other plant species. The objectives of the current proposal are two-fold:The regulation of expression of 17 known SDH isomers in apple as well as total SDH activity will be studied by:Characterizing tissue-specific expression of the SDH isomers in 'Golden Delicious' apple by quantitative RT-PCR in immature and mature leaves, cambium, and roots for comparison to fruit cortex and seed.Determining which SDH isomers are transcriptionally-induced or inhibited in apple tissue by sorbitol or other sugars, and by cultural practices such as pruning and fruit thinning.Assessing the possibility of posttranslational modification by phosphorylation of SDH in response to inductive treatments.Determining the relationship between xylem sorbitol content and fruit cortex SDH expression and activity during fruit set and early fruit growth.The novel role of SDH in stress tolerance of Arabidopsis as a model for species not commonly producing sorbitol will be studied by:Analyzing SDH expression and activity and measuring content of sorbitol and ribitol in all tissues of wild type and sdh knockout mutants in response to abiotic stresses in time course studies for characterization of the development of the mutant phenotype.Assessing the role of ribitol metabolism by SDH in a putative riboflavin biosynthetic cycle during plant stresses.Determining if toxic metabolites are derived from ribitol and if altered content of reactive oxygen species contribute to the sdh knockout mutant phenotype. Determining if UV-C irradiation can be used to elicit the unique mutant phenotype as a more rapid and easily-regulated treatment than drought stress.
Project Methods
Objective 1'Golden Delicious' apple trees in the UK South Farm orchard will be used. In addition, young 'Golden Delicious' trees will be grown in containers if necessary. We are currently developing probes to identify and differentiate among the 17 SDH isomers in the apple genome of this cultivar, the only fully-sequences apple genome available. Preliminary analyses using probes from our prior work with 'Mutsu' apple indicated that the probes used in that work cannot be used to distinguish among the isomers in 'Golden Delicious' (data unpublished), suggesting the partial sequences upon which the probes are based differ among cultivars.Shoots and spurs bearing apple fruit will be defoliated and girdled as described in Archbold (1999) for depriving fruit, immature leaves, and shoot tips of sorbitol. Fruit, shoot tips, cambium, and mature and immature leaves will be collected 2-3 weeks after treatment from control and defoliated/girdled shoots/spurs. Tissues may be frozen immediately in liquid N2 or used in induction studies. Fruit will be sectioned into cortex sections and seed. Roots will be collected from air-layered shoot sections, for induction of adventitious root development, and frozen in liquid N2 also. Frozen tissues will be stored at -80 ºC for subsequent analyses.Tissue-specific and induced expression of SDH isomers by Real Time PCRTissue specific and induced expression of the 17 known SDH isomers will be characterized by RT-PCR by methods described by Nosarzewski and Archbold (2007), using tissues from apple fruit cortex, cambium, roots, immature and mature leaves, and shoot tips following treatments to trees or limbs, and after incubation in control versus polyol-containing solutions for 24 h (Archbold, 1999; Nosarzewski et al, 2004).SDH activity measurementSDH will be extracted and assayed as described (Archbold, 1999; Nosarzewski et al., 2004, 2012).Determination of possible posttranslational modification of SDH If SDH expression and protein are found but activity is not, the possibility of posttranslational modification via phosphorylation will be studied. Protein will be extracted from frozen tissues using either dephosphorylation inhibitors or phosphatase to preserve or remove phosphate groups, respectively, and separated by two-dimensional gel electrophoresis. Protein from these 2D gels will be transferred to PVDF membrane followed by detection by SDH antibody developed in our lab (Nosarzewski et al., 2004) to identify complementary SDH protein spots on the gel (Nosarzewski and Archbold, 2007). On a sister gel, protein spots will be imaged using SPYRO ruby, aligned with the immunoreactive gel, and the spots corresponding to SDH will be precisely excised. Gel fragments will be sent to the Center for Structural Biology proteomic facility at UK. The same analysis will be performed using Arabidopsis SDH protein extracted from leaves prior to and after SDH induction with sorbitol. By comparing SDH isomers obtained from tissues with high SDH activity to those from tissue without SDH activity, a shift in pI values may be evidence of possible phosphorylation. In addition, the separated SDH isomeric proteins will be sent to the proteomic facility at UK to confirm their phosphorylation status and to identify modified residues.Manipulation of xylem collection sap sorbitol content Trees, or branches isolated by girdling at their base, will be defoliated in the fall after harvest and at intervals during spring bud break and early shoot growth to determine if a range of xylem concentrations of sorbitol can be generated. Xylem sap content will be collected from shoot or spur pieces at weekly intervals in the month preceding bloom and ending 2 weeks afterwards. The sap sugar and polyol content will be measured by gas chromatography (Wu et al., 2010). Growth rates of fruit on the trees or branches will be measured, and fruit will be collected for measurement of cortex SDH isomer expression and activity (Wu et. al, 2010).Objective 2Characterizing the development of the unique mutant phenotypeArabidopsis plants will be grown as described by Villadsen and Smith (2004). Wild type and sdh knockout plants will be drought-stressed (Nosarzewski et al., 2012), and sampled at 2-day intervals leading up to the development of the mutant phenotype. Leaf tissues will be analyzed for content of sorbitol and ribitol, expression of the single isomer of SDH present in Arabidopsis, and SDH activity (Nosarzewski et al., 2012).The unique sensitivity of the sdh mutants to ribitol will be studied. During seed germination/incubation on ribitol-containing media (Nosarzewski et al., 2012), seed will be moved at intervals to ribitol-free media to determine if plants can recover and resume germination. Concurrently, seeds will be collected for analysis to determine if unique ribitol-derived and/or ribitol-induced compounds are produced.Assessing the role of SDH in a putative riboflavin cyclePlants of the sdh knockout mutants collected as above in time course studies will be analyzed for riboflavin, lumichrome, FAD, and FMN content by HPLC methods recently developed and tested, modified from Deng et al. (2011).Unique ribitol metabolites and reactive oxygen species in mutant plantsPlants will be fed 14C-ribitol by exogenous application to the leaf surface and/or through the transpiration stream of excised shoots. The fed tissue will be extracted, and the extracts analyzed by HPLC to separate 14C-labelled compounds. Unique compounds will be analyzed by GC-MS. Results using wild type plants will be compared to those using sdh knockout plants.The effect of drought stress on leaf content of reactive oxygen species, including H2O2, ascorbic acid, and glutathione, and related enzymatic activities, including superoxide dismutase, ascorbate reductase, and glutathione reductase, in control versus sdh knockout plants will be measured (Deng and Dong, 2013), using plants collected in time course studies as above.Assessment of UV-C exposure as a treatment to elicit the phenotypePreliminary work indicated that the mutant phenotype was elicited after a 24 h UV-C exposure, although wild-type plants also suffered some injury. This technique would be a much more rapid treatment to use in place of drought stress, but it first must be carefully studied to refine the treatment technique and compared to the drought-induced phenotype, at the whole plant, biochemical, and molecular levels.

Progress 10/01/16 to 09/30/17

Outputs
Target Audience: Nothing Reported Changes/Problems:The unexpected results leading to the development of the herbicide and its commercial potential resulted in spending time with that work rather than the planned work with apple. What opportunities for training and professional development has the project provided?A Ph.D. graduate student has learned all of the critical laboratory techniques as well as experimental design to accomplish her share of the project goals How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?We will continue pursuing commercialization of the herbicide, and studying the role of sorbitol and ribitol in the drought and salt stress responses of tomato.

Impacts
What was accomplished under these goals? Preliminary work indicated that inhibiting sorbitol dehydrogenase (SDH) could inhibit seed germination. An herbicide was developed as a mixture of sorbitol dehydrogenase (SDH) substrates and/or inhibitors, such as natural polyols that includes ribitol, and a growth inhibitive effective amount of an adjuvant. The herbicide was effective at inhibiting seed germination of weed species in lab, greenhouse and field studies. Using a set of SDH antisense lines of tomato (Solanum lycopersicum), we have found that the antisense lines are more sensitive to drought and salt stress and accumulate more sorbitol and ribitol than control plants, and have discovered that the enzyme sorbitol 6-phosphate dehydrogenase is the source of sorbitol in tomato and is expressed in antisense and control plants.

Publications


    Progress 10/01/15 to 09/30/16

    Outputs
    Target Audience:The results were presented to and discussed with fellow horticultural and plant scientists. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A Ph.D. graduate student has learned critical laboratory techniques during the studies. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?Continue studying the anisense tomato lines to look at gene expression patterns of SDH and the aldose reductases during drought stress.

    Impacts
    What was accomplished under these goals? We acquired a set of SDH antisense lines of tomato (Solanum lycopersicum) from their creator, Dr. Yoshinori Kanayama, Tohoku University, Japan, last year. We have studied the role of SDH and sorbitol accumulation in these plants in response to drought and salt stress. Both sorbitol and ribitol acccumulated in stressed plants, more in the antisense than the wild type plants. Increased activity of enzymes responsible for sorbitol biosynthesis, aldose reductases, was also found, and the antisense plants exhibited a unique phenotypic response to drought stress, dying when re-watered, similar to the Arabidopsis drought response phenotype.

    Publications


      Progress 10/01/14 to 09/30/15

      Outputs
      Target Audience: Nothing Reported Changes/Problems:Transgenic tomato (Solanum lycopersicum) with antisense SDH was obtained and has been incorporated into the project parallel to the work with Arabidopsis. What opportunities for training and professional development has the project provided?A Ph.D. graduate student has learned all of the critical laboratory techniques to accomplish her share of the project goals. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?Continue the work with Arabidopsis, and utilize the newly-acquired tomato seed and plants to adress the project goals. Also, we will resume work with apple.

      Impacts
      What was accomplished under these goals? To determine if the phenotype of the Arabidopsis tDNA insertion mutants deficient in sorbitol dehydrogenase (SDH) activity required drought to be sensitive to ribitol, well-watered plants were both sprayed and subirrigated with ribitol, sorbitol, and xylitol. Mutants exhibited foliar damage and senescence typical of the phenotype to ribitol only. Pfizer produces a group of SDH inhibitors for their studies on control of problems associated with diabetes. In response to a request, they gifted an amount of the most effective inhibitor to use in the research. As with the tDNA Arabidopsis mutants, seed germination of wild type Arabidopsis did not occur on ribitol with the inhibitor present although both alone had no effect. In addition, tomato, broccoli, and radish also showed reduced and/or no germination on ribitol with the inhibitor. We acquired a set of SDH antisense lines of tomato (Solanum lycopersicum) from their creator, Dr. Yoshinori Kanayama, Tohoku University, Japan. We have grown these lines, along with wild and null mutant types, to confirm that they do not exhibit detectable SDH activity, and have produced a large number of seed for germination studies.

      Publications


        Progress 02/03/14 to 09/30/14

        Outputs
        Target Audience: Horticultural plant scientists Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Continue characterizing tissue-specific expression of the SDH isomers in 'Golden Delicious' apple by quantitative RT-PCR in cambium, roots, fruit cortex, and seed. Analyze SDH expression and activity and measure content of sorbitol and ribitol in all tissues of wild type and sdh knockout mutants in response to drought stress in time course studies for characterization of the development of the mutant phenotype.

        Impacts
        What was accomplished under these goals? Transcripts of at least seven but possibly nine out of nineteen SDH genes were detected in leaves of 'Golden Delicious'. A phylogram showingthe relationships among the genes was generated using ClustalW2 alignment. Very close similarity among all 19 SDH genes (for some genesonly partial sequences are available) was evident. Three of the SDH genes, MDP0000515106, MDP0000707567 and MDP0000638442, hadalmost identical DNA sequences (exons and intron). Due to the impossibility of designing different primers to separate them, it can only bestated that at least one of the three was constitutively expressed. Thus, at least seven, but possibly nine, SDH genes were expressed inapple leaves. A similar concern was encountered with two other genes, MDP0000190508 and MDP0000285427, which also share identicalsequences, but none of their transcripts were detected in apple leaves. These two genes are closely related to MDP0000292462, the transcriptof which was also not detected.

        Publications