Translational approach to increase phosphate accumulation in two plant species through perturbance of inositol pyrophosphates

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Abstract
Inorganic phosphate (P i ), while indispensable for all biological organisms and a major agricultural macronutrient, is an increasingly limited and nonrenewable resource. Recent studies demonstrate the importance of inositol pyrophosphates (PP-InsPs) in plant P i signaling and homeostasis, however the extent to which PP-InsPs impact plant development is not well understood. We report that transgenic expression of the Saccharomyces cerevisiae enzyme Diadenosine and Diphosphoinositol Polyphosphate Phosphohydrolase (DDP1) in Arabidopsis thaliana and Thlaspi arvense (pennycress) provide a unique translational utility for P i phytoremediation as well as unique germplasm and insight on the long-term impacts of reduced PP-InsPs. Transgenic DDP1 expression in Arabidopsis decreased PP-InsPs, impacted growth and development, and increased P i accumulation leading to P i toxicity. Analysis of P i Starvation Response (PSR) marker genes indicated that the PSR is activated in DDP1 expressing plants. We assessed translational utility through transformation of pennycress, a spring annual cover crop with emerging importance as a biofuel crop, with a DDP1 transgene. Pennycress plants expressing DDP1 showed similar altered P i accumulation phenotypes, suggesting that these plants could potentially serve to remove P i from P i -rich soils. Our study addresses the long-term impacts of PP-InsP reduction on plant growth, as well as establishing a starting material for a unique P i reclaiming cover crop. SIGNIFICANCE STATEMENT: A major challenge to food security is the phosphorus (P) crisis. A global P shortage is imminent based on the misuse of current resources and will be further aggravated by climate change and a lack of policy addressing sustainability. Our work addresses this crisis by investigating the sustained impact of altering inositol pyrophosphates to manipulate plant P accumulation, a strategy that could be used to remediate nutrient-polluted environments.

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