The ABC of fruit-shape formation in the Brassicaceae

Despite the great diversity in plant organ shapes, common principles may underlie shape determination. It has been recognised from the early days of genetics that it is possible to differentiate between gene activities that regulate shape and those that only affect size. Recently, key genetic factors involved in determining shape in domesticated fruit crops such as tomato, melon and pepper have been uncovered. Furthermore, tissue-level models of leaf and petal growth have led to the suggestion that shape depends on patterns of anisotropic growth oriented by a polarity field. We have recently extended these studies by demonstrating that such models also can account for the growth patterns and diversity of three-dimensional fruit shapes.

Angiosperms (flowering plants) evolved during the Cretaceous Period more than 100 million years ago and quickly colonised terrestrial habitats. A major reason for their success was the formation of fruits that protect and nurture the developing seeds. Moreover, a massive range of diversity in fruit shape arose during a relatively short time, which allowed for the development of ingenious ways of fertilisation as well as strategies for efficient seed dispersal. The Brassicaceae family contains a wealth of diversity in fruit morphologies and includes some of our genetically best characterised model plants and important crop species. Thus, the Brassicaceae family provides an ideal group of plants to study how specific shapes are established. Although many genes controlling fruit patterning in the model plant Arabidopsis thaliana have been identified, processes leading to specific carpel and fruit morphologies are still poorly understood. To unravel these processes, we need to compare the growth and morphological development of differently-shaped fruits.

In this project, we will study the molecular and genetic mechanisms that underlie the formation of fruit shape within the Brassicaceae. We will use computational modelling combined with developmental biology and genetics to help understand this diversity. We recently found that simple modulations of a computational model based on experimental data can account for the observed variety of certain fruit shapes among Brassicaceae species. We will expand these studies and include non-model plants with highly diverse fruit shapes. Beyond the fundamental understanding of organ growth, results from this project should help identify strategies for how knowledge of shape and growth can be applied to increase yield of oilseed rape. More generally, understanding the mechanisms underlying organ-shape determination has implications for diverse disciplines ranging from medicine to crop improvement.

It was proposed already in the early days of genetics that common principles underlie the determination of plant organ shape. Our recent work on fruit morphology supports this hypothesis and the proposed project is aimed at identifying and characterising the components involved using Brassicaceae fruit development as a testbed.

Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms. However, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. We recently compared the growth patterns and orientations that determine two different fruit shapes in the Brassicaceae family: the heart-shaped Capsella silicle and the near-cylindrical Arabidopsis silique. Our data revealed that different shapes arise through different patterns of anisotropic growth. These experimental data can be accounted for by a tissue-level mathematical model in which specified growth rates vary in space and time and are oriented by a proximo-distal polarity field.

The model allows us to identify specific activities required to obtain the individual shapes and thus raises two central questions that will be addressed in this proposal: 1) what are the key regulators of fruit shape? and 2) how do they control patterns of growth and shape in the Brassicaceae? To answer these questions, we will combine developmental genetics and modelling to reveal the role of key regulators of fruit shape based on known players and additional factors identified in a recent forward genetic screen. Moreover, we will expand this analysis with the aim to understand the formation of a range of fruit shapes from non-model species.

Beyond the fundamental knowledge on organ growth, this project will lead to the elucidation of basic principles of organogenesis that may be generally conserved across biological kingdoms, while facilitating new directions for improving traits in seed and fruit crops.

Who will benefit from this research and how?
A striking difference between fruits from the model plant Arabidopsis and its close crop relative oilseed rape (OSR) is the length of the apical style. Whereas the Arabidopsis style is short and barely visible with the naked eye, the style of an OSR fruit makes up ~25% of the entire fruit length. In addition to a waste of energy in producing this extended structure, long styles pose a serious problem for seed dispersal (pod shatter) as they often get entangled and rip the pods open under windy conditions. Furthermore, precocious style emergence is a common problem for OSR farmers, when the style elongates prematurely and the stigma is separated from its own anthers. If this occurs during cold and humid conditions when natural pollinators such as insects are absent, flowers will fail to produce seeds. Attempts to reduce style development in oilseed rape therefore have great potential to minimise seed loss and align with UK and EU objectives to reduce crop wastage of OSR. Results from this proposal will point out directions for achieving this through regulation of cell division.

Agricultural industry: Pod shatter leads to an average annual loss of ~15% in seed yield. An increase in oilseed rape yield of 15% would equate to an increase in farm-gate value of £160M in the UK and 2 billion Euro based on 2013 prices if implemented across the EU-28. The industry will benefit from technology development to improve yield and to modify pod shape to minimise seed loss due to unsynchronised seed dispersal (pod shatter). The data obtained here may also point out directions for increasing pod size, seed size and seed number through alteration of hormone levels in specific tissues.

Public: The public would benefit from greater stability in production costs, which would impact on prices in the shops. There are also obvious environmental benefits using the technology described here. OSR has emerged as the second largest oilseed crop with an annual worldwide production of 61 million metric tons of oil (2011) and demand is increasing. For this to be sustainable, seed yield must be dramatically increased through more efficient breeding programmes while at the same time minimising the amount of fertiliser input to protect the environment. We believe the data obtained here will help set out strategies to optimise fertility and reduce dispersal, thus contributing significantly towards such a goal.

What will be done to ensure that they have the opportunity to benefit from this research?

Publications: Results will be published in high-impact scientific journals and the breeding/farming press in a timely fashion. It will also be presented at national and international conferences and trade shows.

Collaborations: The PI has strong connections to the international plant science community. This is reflected in the access to the novel and unique resources described in Case for Support, part 2. We also have strong links to the breeding industry and Brassica crop improvement programmes. The data that we obtain will be of immediate use to these interest groups for example via the BBSRC-funded LoLa project BRAVO (headed by the PI), the Defra-funded Oilseed Rape Genetic Improvement Network (OREGIN) and the UK Brassica Research Community. These networks bring together academic researchers and breeding companies, and the members of OREGIN generate pre-breeding material, and have established a number of populations with the aim to improve traits with relevance to fruit morphology as described in this proposal.

Commercialisation: We are dedicated to promote our results for crop improvement purposes. Informal contacts with industrialists, biotechnologists and related umbrella organisations will be made as soon as any exploitable results are generated. We have tight links with relevant industries and will present results to them either when they visit JIC, at conferences or at visits to the companies.