Exploring natural variation in sucrose metabolism to improve tomato growth and development at sub-optimal temperature

Quy Dung Dinh

Research output: Thesisinternal PhD, WU

Abstract

Tomato is one of the most important vegetable crops in the world. The Netherlands, despite of its relatively small land area, is a leading player in producing and exporting tomato at a global scale. Due to the temperate climate in the Netherlands, the cultivation of tomato, as well as other major vegetables such as sweet pepper and cucumber, is mostly done in greenhouses. In this manner, the growth conditions, such as temperature, lighting, CO2 enrichment, humidity, can be maintained optimally in order to maximize yield of harvestable parts of the crops, i.e. fruits in this case. This type of cultivation in temperate climate areas requires very much energy, mainly for heating which take up 20 – 30% of the total production costs. This high energy consumption for cultivation is deemed to have also a high impact on the environment. Therefore, many efforts have been put into finding solutions to decrease the energy consumption in the greenhouse horticultural sector. For instance, several companies and research institutes have been looking into ways to make novel building materials, optimize light types and intensities to improve photosynthesis efficiency, develop new greenhouse architectures that can become energy-neutral in the future. In this thesis, we looked into the biological side of this issue, in which we set out to understand more about how tomato copes with sub-optimal temperatures (SOT), and explore the genetic variation that can be used to breed new tomato cultivars that perform well at SOT. SOT in this thesis is defined as the temperature below the current economical optimum growth temperature in heated greenhouses in the Netherlands of 19-20°C and above the chilling temperature of 12°C.

In Chapter 1 I presented an introduction about why it is important to develop resilient crops for a sustainable economy in the current situation where the climate changes can have negative impact on food production. The importance of photosynthesis and sucrose metabolism as the direct downstream process on crop growth, development, and yield is discussed. Furthermore, we described in detail sucrose synthases and invertases - two classes of enzymes that directly hydrolyze sucrose molecules, and play a key role in sugar metabolism and transport. As the Netherlands has a temperate climate, reducing the growth temperatures in the greenhouses, i.e. SOT, is one of the options to bring down the energy consumption when cultivating crops with higher growth temperature than ambient temperature. However several studies have shown that plant growth and yield are negatively affected at SOT. I propose that key players in sucrose metabolism should be exploited to help plants to improve the sink strength, plant growth and yield at SOT.

In Chapter 2 we studied the impact of SOT (16/14C° day/night temperatures), in comparison to control temperature (CT, 22/20C°), on plant growth, photosynthetic capacity, and carbohydrate metabolism in a cultivated tomato variety (Solanum lycopersicum cv Moneymaker) and a high altitude wild species tomato (S. arcanum LA385). The study was performed on plants from flowering onset until a later stage of fruit development, in which tomato plants are known to be more sensitive to SOT. We observed that LA385 acclimated well to SOT at the later stage of fruit development in which there were no significant differences in plant growth, photosynthetic capacity, and carbohydrate metabolism, whereas cv Moneymaker was greatly affected by SOT in all the studied parameters. One of the striking findings was the highly active sucrose metabolism in leaf and fruit tissues of LA385 in comparison to that in cv Moneymaker. Overall, the findings in this chapter indicated that LA385 is a potential candidate to be used in a breeding program for new cultivars that can perform well at SOT.

In Chapter 3 we explored the genetic variation in three alleles Susy1/3/4 encoding for sucrose synthase (SUSY). Sucrose synthase is one of the two enzymes directly hydrolyzing sucrose in plants, and deemed to play an important role in sucrose metabolism and plant sink strength. The panel included 84 tomato accessions in total, in which 53 accessions are cultivated tomato and landraces, and 32 accessions are related wild species. As expected, we found fewer variations in Susy1/3/4 in the cultivated and landraces tomatoes, but much more in related wild species. The variation in the deduced amino acid sequences was grouped into 23, 22, and 17 distinct haplotypes for SUSY1/3/4, respectively. Strikingly, in silico analysis of the variations showed that all the known substrate binding sites were highly conserved. Because it has been shown that amino acid changes outside the substrate binding sites can still have a positive effect on enzyme kinetics, we continued with cloning and heterologous expression of a few haplotypes of SUSY1 and SUSY3. Amongst the studied haplotypes, SUSY-haplotype#9, with four alterations, S53A, S106I, E727D, and K741E found in S. arcanum LA385 (the same accession as studied in Chapter 2) and S. arcanum LA2172, showed an improved catalytic efficiency (Vmax/Km) at 16C° compared to the reference SUSY-haplotype#1 found in cv Moneymaker for instance. The findings in this chapter demonstrate that SUSY kinetic properties can be enhanced by exploiting natural variation, and the potential of this enzyme to improve sucrose metabolism and eventually sink strength in planta at SOT.

In Chapter 3, we found five amino acid differences S53A, S106I, Q349L, E727D, and K741E in SUSY3 in the high altitude wild species S. neorickii G1.1601 (SUSY3-haplotype#10) compared to that of the reference SUSY3-haplotype#1 in cv Moneymaker. This SUSY3-haplotype#10 has only one alteration Q349L compared to that of SUSY3-haplotype#9 found in S. arcanum LA385. Since we had a BC3S2 introgression line called Susy3-IL in house which has been identified to carry Susy3 allele of S. neorickii G1.1601, we studied the impact of SOT (16/14C°) in comparison to control temperature (CT, 25/16C°) on plant growth, carbohydrate metabolism, gene expression and enzyme activity of the key enzymes sucrose synthase and invertase in this Susy3-IL in comparison to the recurrent parent tomato S. lycopersicum cv Moneymaker in Chapter 4. The study in Chapter 4 was performed on plants from flowering onset until a later stage of fruit development, in which tomato plants are known to be more sensitive to SOT. Overall Susy3-IL showed an inferior performance relatively to cv Moneymaker in most of the studied parameters at both CT and SOT. The only positive improvement that we observed was that Susy3-IL had a 9% increase in dry mater allocation to fruits compared to that in cv Moneymaker during the fruit ripening phase at CT. However due to the lack of biological replicates, we would need to confirm these results in future study in order to substantiate our initial findings.

In Chapter 5 I discussed all the findings presented in this thesis. I also integrated the findings with the current developments in different research fields, and proposed some new options to extend and exploit the results. I believe that with all the advances in research and development in different fields, and an increase in the interdisciplinary research in this particular field our understanding on how plants respond to SOT will be greatly improved. This will make it possible to screen and integrate the valuable natural variation into current germplasm more efficiently, so that we can eventually breed for new varieties that are more resilient to different sub-optimal growth conditions.

Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Wageningen University
Supervisors/Advisors
  • Trindade, Luisa, Promotor
  • Visser, Richard, Promotor
Award date9 Sep 2020
Place of PublicationWageningen
Publisher
Print ISBNs9789463954211
DOIs
Publication statusPublished - 2020

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