Reflexions, le site de vulgarisation de l'université de Liège
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1 When tomatoes flower 3/13/12 Understanding the mechanisms responsible for tomato plant flowering will enable new selection procedures to be developed in order to obtain even more productive varieties. Researchers in Liege and Louvain-la-Neuve demonstrate the importance of a gene in controlling the number of flowers within a tomato inflorescence. Originally from the north-west of South America where it was domesticated, the tomato rapidly conquered the entire world and arrived in Europe at the beginning of the 16th century. Today it is considered as one of the most important fruits/vegetables (depending on whether we use botanical or culinary language) in the human diet. Various forms and varieties of this plant exist. Thousands of cultivated varieties - called cultivars - in some 170 countries produced more than 125 million tonnes of tomatoes in 2007, according to FAO statistics (United Nations Food and Agriculture Organization). In Europe, each individual consumes around 13kg of fresh tomatoes per year, and 22kg of tomatoes in other forms (cans, sauces, concentrates, juices, etc.)! In short, the economic, agronomic and gastronomic value of the tomato cannot be overstated. However, to keep its place in the sun and retain its position as one of the top three most widely consumed vegetables in the world, after the potato and the sweet potato, the tomato needs to be able to respond to ever increasing demand. To help it do so, scientists have been studying the flowering mechanisms of the tomato plant. To create cultivars producing ever more fruits, it is necessary to understand the genetic bases which lead to the fruits being formed. Claire Périlleux, lecturer and head of the ULg Laboratory of Plant Physiology is one scientist interested in that topic. "Understanding how any crop flowers is interesting because the underlying mechanisms can be used to increase the number of fruits produced by the plant." -1-
2 From producing leaves to flowers Before diving into the genetic mechanisms which control tomato plant flowering, it is important to understand the various stages of flowering in plants in general. "The part of the plant which develops the above ground organs, in other words the stem and the leaves, is called the shoot apical meristem. This tissue is made up of cells which retain a high potential for multiplication and differentiation. These are known as stem cells" explains Claire Périlleux. When the plant is growing, the apical meristem only produces leaves and stem segments. Then, generally following an environmental signal such as day length or light intensity, the plant shifts from the vegetative growing phase to the flowering phase. "This transition to flowering has become autonomous in tomato plants. It was originally a short day plant, but as the result of breeding carried out by horticulturalists, flowering has become independent of day length. However, the process is still accelerated by high light intensity," specifies the researcher. Once flowering has started, depending on the plant, events can occur in one of two ways. In the first case, the apical meristem itself produces a flower, thus using up all its stem cell reserve. Should this occur, only a single flower will be produced, as is the case for a tulip for example. If the plant has to produce several flowers, the apical meristem undergoes certain changes enabling it to both produce a flower and maintain a stem cell reserve in order to be able to produce other flowers. "This is what is known as an inflorescence meristem" states Claire Périlleux. "This is a general mechanism which is found in all plants forming inflorescences such as wheat, vines, tomatoes, etc." The location and way in which stem cells are maintained determine the shape of the inflorescence. -2-
3 The tomato plant's somewhat unusual growth The tomato plant not only forms inflorescences but also presents somewhat unusual and complex flowering. "When the apical meristem produces its first inflorescence, another meristem at the axil of a leaf (an 'axillary meristem') takes on its role for plant growth. This type of growth is known as sympodial growth", says Claire Périlleux. In this way, the axillary meristem goes on to form a stem segment consisting of two or three leaves. It will then in turn produce an inflorescence while another axillary meristem continues plant growth, producing three leaves, etc. "This is why on tomato plants we see seven to ten leaves before the first inflorescence and then two or three leaves, followed by an inflorescence, another two or three leaves and then another inflorescence, and so on. This is also why people are advised to pinch their tomato plants so they stop producing inflorescences and so that the first fruits can grow" continues the scientist. In order to achieve even greater productivity, some horticultural companies would like to obtain cultivars which only produce two leaves between each inflorescence. In an article published in 2008 in the journal Plant Physiology (1), Claire Périlleux and her colleagues described the expression of a gene which is of great interest to these horticultural companies. The Self Pruning gene (SP) in tomatoes prevents lateral meristems from flowering too quickly. It is thus 'because' of this gene that the plant produces three leaves before the next inflorescence. It should be stressed that the orthologue gene of SP in Arabidopsis, called TFL1 (for Terminal Flower 1) does not play the same role. "In this model species, TFL1 acts so that the apical meristem does not flower but becomes inflorescential, i.e. it maintains a reserve of stem cells to produce flowers indefinitely", explains Claire Périlleux. -3-
4 One question remains unanswered in the scientists' minds: what prevents the tomato plant's stem cells from being used up? If it is not SP, what does play this role in the plant? This is the question which Claire Périlleux and Johanna Thouet, a doctoral student in the ULg's Laboratory of Plant Physiology, try to address, alongside researchers from the Catholic University of Louvain-la-Neuve, in a new article published in the journal PLoS ONE (2). The unexpected role of the JOINTLESS gene "In plant biology, many things have been discovered from the study of mutants" says Claire Périlleux. "Given the agronomical importance of the tomato plant, mutants were obtained not as the result of experimental manipulations but through selection programmes, because they presented interesting characteristics or because they grew well." This is the case of the Jointless variety. It has the advantage of not having an abscission zone at the fruit peduncle. "This fragile zone allows the fruit to fall when it is ripe, but horticulturalists prefer to pick the fruit directly from the plant" indicates Claire Périlleux. By taking a closer look, scientists realised that the lack of an abscission zone was not the only 'abnormality' which Jointless cultivars presented. "The inflorescence meristems of this mutant produced one, two or three flowers, and then go on to produce more leaves!" says the researcher. "This is an abnormal developmental -4-
5 programme because once a meristem produces an inflorescence, normally it doesn't produce any more leaves". In the context of their new study, Claire Périlleux and her colleagues created a series of double mutants to understand the role of these genes and how they interact to regulate the formation of inflorescence in tomato plants. "The most interesting and unexpected result that we have seen concerns a double mutant involving the JOINTLESS gene" she reveals. "When a mutation of this gene is combined with a mutation of the Single Flower Truss (SFT) gene, the tomato plant forms a terminal flower, exactly as when the TFL1 is mutated in Arabidopsis!" These results show that the JOINTLESS gene is involved in maintaining the stem cells necessary for the tomato's inflorescence development. But it does not act alone: "It is likely to be the result of a complex interaction between different genes including Single Flower Truss which encodes the mobile protein FT" (see the article : The Cocktail of a Flowering). How many flowers per inflorescence? The scientists then looked at where the JOINTLESS gene was expressed in order to see whether this was coherent with the role which they had proposed. "This gene is only expressed in the part of the inflorescential meristem which remains undifferentiated, i.e. the part which does not become a flower" reveals Claire Périlleux. This expression pattern confirms that JOINTLESS is involved in the maintenance of stem cells within this type of meristem. According to the researcher, JOINTLESS acts as an inhibitor of another gene, called FALSIFLORA, which is required for the formation of the flower. -5-
6 In fact, the mutation of the Single Flower Truss gene alone sometimes provokes the appearance of a terminal flower, but not always. "The double mutant jointless x single flower truss, enables a strict and reproducible phenotype to be obtained" specifies Claire Périlleux. "The mobile protein encoded by SFT moves from the leaves of the plant to the inflorescence meristem, where it activates genes which, in combination with JOINTLESS, control the number of flowers which the inflorescence will initiate". This new information may be valuable to the horticultural world, as the number of fruits produced by a tomato plant depends directly on the number of flowers previously formed. These results have already attracted the attention of a Dutch company which wishes to use them to model tomato flowering in order to make predictions. Could this be the start of a flourishing collaboration? (1) Thouet, J., Quinet, M., Ormenese, S., Kinet, J.-M. and Périlleux, C., Revisiting the involvement of SELF PRUNING in the sympodial growth of tomato. Plant Physiology, 148, (2) Thouet, J., Quinet, M., Lutts, S., Kinet, J.-M. and Périlleux, C., Repression of floral meristem fate is crucial in shaping tomato inflorescence. PLoS ONE 7(2): e doi: /journal.pone
The Plant Cell, November. 2017, American Society of Plant Biologists. All rights reserved
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