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Kalbfuß, Nils; Strohmayr, Alexander; Kegel, Marcel; Le, Lien; Grosse-Holz, Friederike; Brunschweiger, Barbara; Stöckl, Katharina; Wiese, Christian; Franke, Carina; Schiestl, Caroline; Prem, Sophia; Sha, Shuyao; Franz-Oberdorf, Katrin; Hafermann, Juliane; Thieme, Marc; Facher, Eva; Palubicki, Wojciech; Bolle, Cordelia und Assaad, Farhah F. (2022): A role for brassinosteroid signalling in decision-making processes in the Arabidopsis seedling.
In: PLOS Genetics 18(12), e1010541

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Abstract

Plants often adapt to adverse conditions via differential growth, whereby limited resources are discriminately allocated to optimize the growth of one organ at the expense of another. Little is known about the decision-making processes that underly differential growth. In this study, we developed a screen to identify decision making mutants by deploying two tools that have been used in decision theory: a well-defined yet limited budget, as well as conflict-f-interest scenarios. A forward genetic screen that combined light and water withdrawal was carried out. This identified BRASSINOSTEROID INSENSITIVE 2 (BIN2) alleles as decision mutants with confused phenotypes. An assessment of organ and cell length suggested that hypocotyl elongation occurred predominantly via cellular elongation. In contrast, root growth appeared to be regulated by a combination of cell division and cell elongation or exit from the meristem. Gain- or loss- of function bin2 mutants were most severely impaired in their ability to adjust cell geometry in the hypocotyl or cell elongation as a function of distance from the quiescent centre in the root tips. This study describes a novel paradigm for root growth under limiting conditions, which depends not only on hypocotyl-versus-root trade-offs in the allocation of limited resources, but also on an ability to deploy different strategies for root growth in response to multiple stress conditions. Author summary The ability to grow in response to limiting, adverse conditions is a survival strategy unique to plants. This study addresses the tight regulation of differential growth in plants, and how growth is achieved under multiple stress conditions, in the absence of a carbon or energy source. We design a screen to identify decision-making mutants by deploying two tools that have been used in decision theory: a well-defined yet limited budget, as well as conflict-of-interest scenarios. We also apply a new combination of stress factors: water stress and light deprivation. Our manuscript addresses tradeoffs in hypocotyl versus root growth, with an emphasis not on growth arrest but rather on enhanced growth responses to abiotic stress factors. Our findings challenge the widely accepted view that root growth correlates with meristem size;we propose alternative root growth strategies for adaptation to adverse, limiting conditions. Our genetic screens have identified the BIN2 clade of shaggy-like kinases as playing a central role in decision-making in the seedling. We address the controversy in the literature regarding brassinosteroid function at a cellular level. This we do by exploring the role of BR signalling in the regulation of cell elongation and geometry in response to abiotic stress cues. Our findings suggest that BIN2 and its homologues are required for the decision as to which growth strategy to adopt under different environmental conditions.

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