Control of dissected leaf form in the Arabidopsis thaliana relative Cardamine hirsuta

Lead Research Organisation: University of Oxford
Department Name: Plant Sciences

Abstract

A key problem in biology is to understand how different organisms come to have different forms. In plants this variation in form is obvious in the many different leaf shapes one sees during a walk in the park. Leaves are also interesting to study because they play a key role in the food chain being the main photosynthetic organs of land plants and thus responsible for CO2 fixation in terrestrial ecosystems. For these reasons, understanding how diversity in leaf form in generated is of considerable interest to scientists. To study this problem we work with the hairy bittercress (Cardamine hirsuta), which is a plant that has leaves fully subdivided into small leaflets. The presence of leaflets makes this plant very different to its close relative the thale cress (Arabidopsis thaliana), which has entire, undivided leaves. We already know a lot about how entire leaf shape is produced in A.thaliana because it is easy to grow and do experiments with. Hairy bittercress is also very easy to work with in the lab, so we will use it to understand how leaflets are produced, what controls their number, and ultimately why this plant makes leaflets whereas its relative the thale cress does not.

Technical Summary

We will study mechanisms controlling leaflet development and natural variation in leaflet number in Cardamine hirsuta, which is a dissected leaf relative of the model organism Arabidopsis thaliana. We will do this by using clonal analysis to directly examine which cells within the leaf are responsible for leaflet production and by investigating whether regulated cell division activity controls leaflet development. We will also map genes controlling natural variation in leaflet number by performing QTL analysis in natural variants of C. hirsuta. We will study whether these genes, act to change the position, timing or rate of leaflet initiation. This work will help understand how the reconfiguration of leaf growth and development pathways during evolution has produced different leaf forms.

Publications

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Description 1. We demonstrated that C.hirsuta leaflets are derived from a novel axis of growth arising from division of a small population (2-4) of leaflet founder cells at the leaf margin. These axes are formed in response to activity maxima of the hormone auxin. Analysis of a Cyclin B1::GUS reporter gene confirmed the existence of such cell division foci at the leaf margin and moreover revealed an unexpected centrifugal cell division arrest front in C.hirsuta in contrast to a basipetal arrest of cell division shown during A.thaliana leaf development. These findings indicate that distinct cell division dynamics are instrumental in generation of simple versus dissected leaf forms. Consistent with this idea blocking cell division by broad expression of a cyclin dependent kinase inhibitor (CKI) compromised leaflet formation. We also explored the relationship of regulated growth and leaflet formation in tomato: a plant where the dissected leaf form evolved independently to C.hirsuta, and showed that a DELLA growth repressor is required for defining the correct timing of leaflet formation. Thus, species-specific control of the timing and direction of cell division activity likely contributed to sculpting dissected leaf forms.

2. We generated two sets of C.hirsuta Recombinant Inbred Lines (RILs) and used those to construct a C.hirsuta linkage map and subsequently to map QTLs controlling natural variation in leaflet number and four EMS induced mutants perturbing leaflet development.

3. We showed that CUP SHAPED COTYLEDON GENES (CUC) are required for leaflet number and positioning likely acting in a feed forward loop with KNOTTED1 like homeobox (KNOX) genes. Further we demonstrated that KNOX activity in leaflet formation is contingent on the ability of the basal part of the leaf to organize the aforementioned auxin activity maxima.
Exploitation Route Fundamental information on plant growth that broadens the knowledge for crop improvement.
Sectors Agriculture, Food and Drink