Morphogenesis in plants is often robust, resulting in a reproducible organ size and shape across organisms. In a new study, Adrienne Roeder and colleagues investigate this robustness in the developing Arabidopsis thaliana sepal. They find that the robustness is not affected by changes in the amount of cell division, but the variability of cellular growth rate must be uncorrelated or anti-correlated for robust development to occur. To find out more about the work, we caught up with first author Isabella Burda and corresponding author Adrienne Roeder, Associate Professor at Cornell University, USA.

Adrienne Roeder (left) and Isabella Burda (right)

Adrienne, can you give us your scientific biography and the questions your lab is trying to answer?

AR: I am an Associate Professor in the Weill Institute for Cell and Molecular Biology and the School of Integrative Plant Sciences, Section of Plant Biology at Cornell University. I earned my B.S. in Biological Sciences with a minor in Mathematical and Computational Sciences from Stanford University in 1999. I earned my PhD from the University of California, San Diego, working with Martin Yanofsky in 2005. I completed a postdoctoral fellowship at Caltech with Elliot Meyerowitz before starting my own lab studying cell size and organ size in Arabidopsis flowers using a computational morphodynamics approach. I have a longstanding interest in plant cell and developmental biology. My lab studies how cell size and organ size are regulated in plants. Specifically, we study how plants generate cells with diverse sizes, ranging from giant to small, through regulating endoreduplication. On the flip side, we also study how plants form organs, such as sepals, with reproducible size despite variability of cells in their size, growth and division. Strikingly, my lab is finding that plants use stochasticity or randomness to produce robustness and regularity.

Isabella, how did you come to work in the lab and what drives your research today?

IB: I am a PhD student in the molecular biology and genetics department at Cornell University. When rotating in different labs in my first year, I really enjoyed that research in the Roeder lab was driven by big picture questions and concepts, and I also enjoyed that the lab environment was very enthusiastic. Now, curiosity about morphogenesis, and how both molecular-scale and organ-scale factors affect development, drives my research.

What is the background of the field that inspired your work?

AR: Many plant organs start as a similarly shaped group of cells that grows out of the meristem, yet mature plant organs have diverse shapes. Morphogenesis must create these shapes, even though plant cells are stuck together by the cell wall, which prevents cells from swapping positions relative to each other. Further, plant cells do not contract, and rarely undergo apoptosis. Despite these challenges, morphogenesis is often robust, meaning that organ size and shape is a reproducible outcome. Previously it was found that in robust development there is heterogeneity in cell growth rate, which is counterintuitive to the uniformity in mature organ size and shape. Further, a decrease in cell growth heterogeneity leads to a loss of robust development of organ size and shape. This suggests that heterogeneity contributes to robust development, and we sought to understand how heterogeneity at a cell-scale led to robustness at an organ-scale.

We sought to understand how heterogeneity at a cell scale led to robustness at an organ-scale

Can you give us the key results of the paper in a paragraph?

AR: We find that robust sepal morphogenesis occurs when fluctuations in growth rate are uncorrelated. We also find that growth rate fluctuations and robust development are not affected by changing the amount of cell divisions. In a growing organ with uncorrelated fluctuations in cell growth rate, the cumulative growth approaches the target growth rate over time and over a larger space. This leads to reproducible or robust organ size and shape.

Isabella, when doing the research, did you have any particular result or eureka moment that has stuck with you?

IB: For a while, we had trouble quantifying the local growth heterogeneity around the target growth rate, because the target growth changes at different developmental stages. The ‘eureka’ moment was when Fridtjof Brauns (University of California, Santa Barbara) was able to model and subtract the target growth rate at each time interval, leaving the local-scale fluctuations. Then we could quantify changes in growth fluctuations over time and spatially in the tissue, and then compare the heterogeneity in the fluctuations between genotypes. This analysis led us to the conclusion that spatiotemporal averaging occurs because cell growth fluctuations are not correlated.

One sepal of a developing inflorescence of the lgo-2 mutant is lineage tracked over two time points. Meshes matching the curved surface of the sepal epidermis were made using the software MorphoGraphX. The colours of the cell labels mark the same cell lineage at both time points. Scale bar: 50 µm. Image credit: Isabella Burda.

One sepal of a developing inflorescence of the lgo-2 mutant is lineage tracked over two time points. Meshes matching the curved surface of the sepal epidermis were made using the software MorphoGraphX. The colours of the cell labels mark the same cell lineage at both time points. Scale bar: 50 µm. Image credit: Isabella Burda.

And what about the flipside: any moments of frustration or despair?

IB: When I crossed the LGO overexpression p35S:mCitrine-RCI2A (membrane marker) line with the ftsh4-5 mutant, the expression of membrane marker was silenced in all the double mutants. Silencing is a somewhat common occurrence in Arabidopsis, especially with promoters that cause high expression levels, but is frustrating nevertheless! Eventually it was the last genotype that I still needed to time-lapse image, and I did not have the plant line with the membrane marker. I ended up having to transform the membrane marker into the plants again, and screen for a new insertion line that expressed the membrane marker.

Why did you choose to submit this paper to Development?

AR: Since I was an undergraduate reading papers, Development has been one of my favourite journals. I particularly appreciate the recent emphasis on quantitative analysis and modelling of development, which is a good fit for this paper.

Isabella, what is next for you after this paper?

IB: Next, I am following up on the cellular mechanism behind uncorrelated growth fluctuations in wild type and correlated growth fluctuations in ftsh4.

Adrienne, where will this story take your lab next?

AR: We are working on piecing together the overall picture of the principles and mechanisms generating robustness and how they relate to one another. Spatiotemporal averaging is a key part of that picture.

Finally, let's move outside the lab – what do you like to do in your spare time?

IB: In my spare time I run and train for races. In college, I was on the cross-country and track team, and I still enjoy the sport. Cornell is in the Finger Lakes region of New York state, which has many beautiful places to run.

AR: In my spare time I play with my two cats, Squeak and Lovebug, hike, and read fiction.

I.B. & A.R.: Genetics, Genomics, and Development Graduate Program, Cornell University, Ithaca, NY 14850, USA; Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY 14850, USA; School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, NY 14850, USA.

E-mail: [email protected]

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Robust organ size in Arabidopsis is primarily governed by cell growth rather than cell division patterns
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Development
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