Bilateral BBSRC-FAPESP: Cellular and regulatory basis for early plant organ growth

Lead Research Organisation: John Innes Centre
Department Name: Cell and Develop Biology

Abstract

A central problem in Biology is to understand how genes cause organs to grow to a specific shape and size. Plants are convenient to address this question because their overall growth results primarily from the increase in cell numbers and increase in the size of individual cells (cell movement and "pruning" by cell death do not need to be considered). In addition, understanding organ growth in plants offers a clear path to practical use through the rational manipulation of crop growth and yield.

A major bottleneck for understanding plant growth, however, is that although we know several genes that control the overall size and shape of organs, we do not understand what processes these genes control within cells (such as cell division or increase in cell mass) to result in a net effect on the total size and shape of organs. We aim to answer this question, by studying the early stages of floral organ development in the model species, Arabidopsis.

Unprecedented opportunities to address the question above arise from two recent developments. One is the establishment of methods that allow quantitative, 3D analysis of cell geometry and cell division in growing organs. Using these methods, the UK partner in this project has recently found that a key regulator of organ growth, called JAGGED (JAG), has an unanticipated role in co-ordinating cell volume with cell division in developing organs. The second is the development of techniques for detection of all genes controlled by a given regulatory gene, at well-defined stages of organ formation - this can reveal the repertoire of cellular functions that are controlled by a regulatory gene. Our Brazilian/Dutch partners have been developing these methods and applying them to understand the role of genes that control floral organ development.

Taking advantage of the complementary expertise, resources and biological interest of the UK and Brazilian/Dutch partners, we will extend both approaches to a key set of genes that control plant organ growth: JAGGED (JAG), AINTEGUMENTA (ANT) and CIN-TCP genes. We will test whether the co-ordination between cell size and cell division is a key feature of targeted by these genes at the early stages of organ growth. We will also test whether these genes target specific steps in cell division and clarify how the activities of these regulatory genes are combined during organ growth. Finally, we will identify the sets of genes controlled by JAG and CIN-TCP genes in the early stages of organ development - this will show to what extent the function of these genes overlap, and reveal the key cellular functions targeted by these genes to determine how the organs grow.

One of the current priorities in developmental biology is to develop computer models that can simulate and predict the way organs and organisms grow. Addressing the questions in this proposal will be essential for connecting these models with molecular mechanisms that can be controlled experimentally. Ultimately, this knowledge will allow rational modification of plant organ growth, which has an obvious impact on crop performance. In addition to addressing a fundamental biological question with strategic relevance, our work will establish new and mutually beneficial long-term scientific links between UK and Brazilian institutions.

Technical Summary

To understand how the activity of regulatory genes within cells is translated into the shape and size of plant organs, we aim to reveal what growth-limiting cellular processes (e.g. cell cycle control, cytoplasmic growth, cell expansion) are targeted by regulatory genes that control plant organ growth. For this, we will take advantage of two recent developments. First, the establishment of methods that combine detection of newly synthesized DNA with quantitative analysis of cell geometry in 3D images of developing organs. Using these methods, the UK applicant has revealed an unanticipated role for the regulatory gene JAGGED (JAG) in co-ordinating cell volume with cell division in organ primordia. Second, the application of ChIP-seq on developmentally synchronised floral organs. The Brazilian applicant and Dutch collaborators have been developing these methods to understand the role of CIN-TCP genes in floral organ growth. We will combine the complementary expertise, resources and biological interest of the UK and Brazilian/Dutch partners to study the function of a key set of growth regulatory genes: JAGGED (JAG), AINTEGUMENTA (ANT) and CIN-TCP genes. We will test whether coupling of cell size and cell division is a key feature of primordium growth that is targeted by multiple regulatory genes. We will also test whether these genes target particular steps in cell division and clarify the genetic interactions between JAG, ANT and CIN-TCPs in the control of cell growth and division in developing organs. Finally, we will use ChIP on synchronised organ primordia to identify the sets of genes directly controlled by JAG and CIN-TCPs in the early stages of organ development.

In addition to addressing a fundamental question with long-term impact through the rational manipulation of crop growth and yield, our work will establish mutually beneficial scientific links between the UK and Brazil.

Planned Impact

This project will benefit five main non-academic beneficiaries, in the following ways:

1. Breeders will benefit from knowledge that will facilitate the selection of candidate genes for improving crop growth and yield by conventional or transgenic approaches. The expected time frame for this beneficial impact will be 5-10 years after the start of the project.

2. Agricultural businesses will benefit from our work indirectly, through future use of the resources and knowledge made available to academic peers and to breeders. The most obvious potential benefit will be crop varieties with increased yield through changes in developmental constraints on growth. The channels to these beneficiaries will be breeders, as mentioned above, and licensing of patented knowledge through PBL Technologies (http://www.pbltechnology.com/). The time frame for this type of impact is expected to be 10-20 years.

3. Industry: depending on the career path of the person working on the project, the industrial sector may also benefit from personnel with unique training. This will include theoretical and technical knowledge ranging from molecular genetics to advanced biological imaging and image analysis, communication skills including the clarity and rigour required to write papers and talk at scientific meetings, and a network of contacts spanning academia and breeders (3-4 years).

4. The general public will benefit from interacting with researchers working in areas of public concern, such as food security and genetic modification. The channels for interaction with the public include the Teacher-Scientist Network (http://www.tsn.org.uk/) and presentations at the Friends of John Innes Society (http://www.jic.ac.uk/corporate/friends/index.htm) (3-4 years).

5. BBSRC will benefit because the project is directly relevant to the research priority Systems Biology. In addition, the project will establish concrete links between leading scientific institutions in Brazil and the UK; further development of these links is likely to open new opportunities in the BBSRC priority areas of bioenergy and food security (3-10 years).

Publications

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Sablowski R (2014) Interplay between cell growth and cell cycle in plants. in Journal of experimental botany

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Sablowski R (2015) Control of patterning, growth, and differentiation by floral organ identity genes. in Journal of experimental botany

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Sablowski R (2013) Roots of beauty. in Nature reviews. Molecular cell biology

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Schiessl K (2014) Arabidopsis JAGGED links floral organ patterning to tissue growth by repressing Kip-related cell cycle inhibitors. in Proceedings of the National Academy of Sciences of the United States of America

 
Description A central problem in Biology is to understand how genes cause organs to grow to a specific shape and size. In plant biology, this question also has practical implications for crop improvement. In this project, we addressed this question by studying the early stages of floral organ development in the model species, Arabidopsis. We found that:

1. One of the best known genes that control growth of shoot organs (called JAGGED) promotes organ growth by allowing cells to proceed into DNA synthesis - in other words, entry into DNA synthesis isa limiting factor for tissue growth that is regulated to produce the size and shape of plant organs. These findings were published in Schiessl at al., Proc. Natl. Acad. Sci. USA, 111: 2830-2835, 2014.

2. We also found that JAGGED regulates the way cell growth is coordinated with cell division. Coordination of cell grwoth and division determines cell size. Detailed analysis of this process in the shoot meristem revealed that cell sizes and cell size uniformity are important to achieve the resolution necessary to develop plant structures at a scale just a few cells across, such as the boundaries between new organs and the meristem. This is analogous to the way appropriate pixel sizes are necessary to render detail in digital images. This work was published in Serrano-Mislata et al, Current Biology 25: 2991-2996, 2015.

In addition to addressing a fundamental biological question with strategic relevance, our work will established new and mutually beneficial long-term scientific links between UK and Brazilian research institutions.
Exploitation Route This project is fundamental in nature, so its impact will be long-term. The area of science we helped to advance (control of plant tissue and organ growth) has clear importance for the improvement of crop performance.
Sectors Agriculture, Food and Drink

URL http://www.sciencenewsline.com/news/2015103001070006.html
 
Description This project is fundamental in nature, so its impact will be long-term. The area of science we helped to advance (control of plant tissue and organ growth) has clear importance for the improvement of crop performance. The project also helped to develop scientific interactions between the UK and Brazil.
First Year Of Impact 2014
Sector Agriculture, Food and Drink
Impact Types Cultural

 
Title Image analysis software 
Description Tracking and analysing quantitatively the growth and division of cells in three dimensions is a significant challenge. To track cell growth and division in time-lapse confocal images of Arabidopsis inflorescence apices, we developed a package of Python scripts and Fiji macros to landmark, segment, locate, track and measure cells in 3D (3D_meristem_analysis). The package with instructions and annotated source code is available as Supplemental Software in a paper by Serrano-Mislata et al. (http://dx.doi.org/10.1016/j.cub.2015.10.008). 
Type Of Technology Software 
Year Produced 2015 
Open Source License? Yes  
Impact The software has significantly changed the way we approach our research and has opened new research directions. For example, it is being used to show how regulatory genes control the rates and orientation of tissue growth during the early stages of stem development. The method is also being used for the quantitative analysis of floral bud growth in cereals, in collaboration with Scott Boden (JIC) - this is expected to impact on research that is directly relevant to crop yield. 
URL http://dx.doi.org/10.1016/j.cub.2015.10.008
 
Description NRP/FAPESP, UK-Brazil Plant Sciences Workshop 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact This workshop held in Norwich between 23-25 January 2013. The aim was to strengthen interactions between scientists across the Norwich research Park and scientists in Brazil, principally in the São Paulo area, that are engaged in Plant Science Research.

The meeting included talks from 19 Brazilian scientists and 20 project leaders from the Norwich Research Park (from the John Innes Centre, University of East Anglia and The Genome Analysis Centre) and covered the following key areas of impact and complementary science to be pursued in bilateral collaborations: Analysis and biology of complex genomes, Crop improvement, Plant Reproductive Biology, Sugar metabolism and cell walls, Natural products, Molecular approaches to study disease resistance in plants, Structural Biology and Frontier approaches: Advanced imaging and mathematical modelling.

The workshop was co-funded by FAPESP, UEA and JIC, and was organised by Robert Sablowski (JIC), Marie-Anne van Sluys (FAPESP) and Colin Morgan (UEA).


Following the workshop, ideas for eleven different potential collaborations between UK and Brazilian Scientists were further developed with the aim to apply for joint funding.
Year(s) Of Engagement Activity 2013