Award details

Nuclear calcium regulation of plant development

Reference	BB/P007112/1
Principal Investigator / Supervisor	Dr Myriam Charpentier
Co-Investigators / Co-Supervisors
Institution	John Innes Centre
Department	Cell and Develop Biology
Funding type	Research
Value (£)	1,012,044
Status	Completed
Type	Fellowships
Start date	01/03/2017
End date	31/12/2022
Duration	70 months

Abstract

Root legume symbioses are the only plant system with a well-defined nuclear calcium signal. I have used this system to dissect nuclear calcium signalling in plants. I demonstrated the first nuclear calcium channels in plants, encoded by cyclic nucleotide gated channels (CNGC)15s, which form a complex with the potassium permeable channel, DMI1, to create a large channel complex capable of generating symbiotic nuclear calcium oscillations. These channels are conserved across many plant species, including non-symbiotic plants, and from this I concluded that this channel complex must play additional functions beyond the establishment of symbiotic associations. To assess this, I generated Arabidopsis mutants in DMI1 and CNGC15 in Arabidopsis. Mutations in Arabidopsis CNGC15 show defects in root development and fertility, as well as other defects yet to be validated. Interestingly Arabidopsis dmi1 mutants also show root developmental defects, although the effects are opposite to those observed in cngc15. These preliminary analyses imply that the channel complex that I discovered in legumes plays broader roles in plant development. I propose that this channel complex controls all aspects of nuclear calcium signalling in plants and thus through these analyses, I will be able to define where and when nuclear calcium signalling is important during plant development and environmental responses. My fellowship proposal focuses on the role of CNGC15 and DMI1 during root development, both root growth and symbiotic associations in legumes. I have demonstrated that phytohormones activate nuclear calcium responses in Arabidopsis root meristematic cells. In my proposed fellowship I will dissect the detailed mechanism of action of the DMI1/CNGC15 channel complex and its broader function during root development.

Summary

Calcium signalling is essential for growth and development, in both plants and animals. In animals nuclear calcium release is a potent regulator of neuronal gene expression and of cell proliferation. Nuclear calcium signalling is also known to be essential in legumes to promote associations with nitrogen fixing bacteria and phosphate delivering arbuscular mycorrhizal fungi. Legumes are among the world's most important agricultural food crops that are beneficial to billions of farmers and consumers worldwide and provide an essential aspect of natural soil enrichment of organic nitrogen compounds. The mechanisms of plant nuclear calcium signalling were poorly understood. During my work I have used the symbiotic associations in legumes as a platform to dissect plant nuclear calcium signalling. Using a wide range of approaches, I discovered a number of ion channels located at the nuclear envelope that are responsible for symbiotic nuclear calcium release. Among them, I defined the first plant nuclear-associated calcium channels encoded by cyclic nucleotide gated channels (CNGC15s). The CNCG15s sit at the nuclear envelope in a complex with a potassium permeable channel (DMI1), also required for the generation of the symbiotic nuclear calcium signals. Interestingly, CNGC15s and DMI1 are conserved across all land plants, including non-symbiotic species, strongly suggesting that they have other functions during plant development. Consistent with this I have found a number of defects in Arabidopsis lines mutated in CNGC15 and DMI1, that include root developmental defects. I propose that my research in legumes has revealed the generic plant machinery involved in the regulation of nuclear calcium release. By studying the components that regulate nuclear calcium release I will be able to understand when and where nuclear calcium signalling is important. My proposal will focus on the role of nuclear calcium signalling during root development, both root growth and associations with symbiotic microorganisms. Consistent with a function for CNGC15 and DMI1 in root development I have observed nuclear calcium responses in Arabidopsis root meristematic cells during their response to the phytohormones auxin and cytokinin. These calcium responses are mechanistically different from the nuclear calcium signals observed in legumes during symbiotic associations. My proposed research integrates molecular biology, genetics, cell biology, chemistry, electrophysiology and mathematical modelling to investigate how CNGC15-DMI1 regulates nuclear calcium release leading to plant developmental processes. It will use a large collection of Arabidopsis mutant and transgenic lines, that I have already generated, with a panel of nuclear calcium sensors allowing detection of nuclear calcium signals in an array of Arabidopsis mutants. My work will dissect the functions that nuclear calcium signalling plays in root developmental processes and how diverse nuclear calcium signals are encoded. Finally, through a combination of transcriptomics and mutant screens, I will be uniquely poised to decipher the downstream signalling components associated with nuclear calcium signalling during root development.

Impact Summary

The outcomes of the proposed research will be of significant benefit to farmers and plant breeders as it has the potential to impact on crop yield and thereby to the UK public in general by contributing to UK's economic competitiveness. Over 800 million people lack adequate access to safe and nutritious food. The world faces an even greater crisis in food security as expected global population growth to over 9 billion by 2050, is coupled with global climate change. On the issue of global warming, we have underestimated extreme climate fluctuations at the decadal time scale, which will influence UK and worldwide food security by creating unpredictable food shocks. It is urgent to develop new strategies to sustainably enhance worldwide agricultural production. Thus, understanding plant development, and how plants can integrate diverse environmental stimuli into developmental responses, is essential to improve resilience in crop production. My work will establish a molecular underpinning to the understanding of root development, a strategic important research area. Calcium (Ca2+) is a universal regulatory molecule and intimately couples primary biotic and abiotic signals to many cellular processes allowing plant development and adaptation to environmental changes. My proposed research is at the leading edge of studies in plant development and nuclear Ca2+ signalling, providing exciting, new insights into the mechanisms of nuclear Ca2+ signal transduction during plant development. I will unravel the regulatory mechanisms of the central regulator of nuclear Ca2+ signal, which is at the core of multiple developmental processes such as root growth and fertility, targets for plant breeders to improve crop production. By elucidating the mechanism of plant nuclear Ca2+ generation, this proposed research will position the UK as the leader in a new research area. Beyond the excellence, the outcome of this proposed research, combined with the new technology of genome editing, has the potential to be directly transferred to the main crops constituting the world's breadbasket (eg. wheat, maize) and major crops in developing countries (eg. rice, millet, sorghum). This could impact the production at multiple levels, from the biggest farming regions in UK, USA and Russia to the small farmers in sub-Saharan Africa. In summary, the proposed project opens a new research area in plant sciences by determining how nuclear Ca2+ signals are regulated to influence plant growth. This research will have strong social, economic impacts involving UK competitiveness and global food security.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Plant Science
Research Priority	X – Research Priority information not available
Research Initiative	Fellowship - David Phillips Fellowship (DF) [1995-2015]
Funding Scheme	X – not Funded via a specific Funding Scheme

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