Review

A plant’s diet, surviving in a variable nutrient environment

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Science  03 Apr 2020:
Vol. 368, Issue 6486, eaba0196
DOI: 10.1126/science.aba0196

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Root growth regulation by requirement

Plant productivity depends on the elemental nutrients nitrogen and phosphorus, which are drawn from the soil. Oldroyd and Leyser review how root growth patterns adjust according to the physiological needs of the above-ground plant. Systemic signals, including small peptide signals, mediate communication between the shoot's needs and the root's supply.

Science, this issue p. eaba0196

Structured Abstract

BACKGROUND

Although plants are dependent on the capture of a number of elemental nutrients from the soil, the principal nutrients that limit plant productivity are nitrogen (N) and phosphorus (P). Acquisition of these nutrients is essential for crop performance, but levels of these nutrients in most agricultural soils limit productivity. Therefore, these nutrients are typically applied at high concentrations in the form of inorganic fertilizers to support food production. However, overuse of fertilizers allows environmental nutrient release, which reduces biodiversity and contributes to climate change. Many farmers around the world lack the financial resources to access fertilizers, and their crop productivity suffers as a consequence. A more sustainable and equitable agriculture will be one that is less dependent on inorganic fertilizers.

ADVANCES

Accessibility of N and P in the soil is affected by many factors that create a variable spatiotemporal landscape of their availability, both at the local and global scale. Plants optimize uptake of the N and P available by modifications to their growth and development and through engagement with microorganisms that facilitate their capture. Where N and P are ample, the ratio of root:shoot biomass allocation can be low, with minimal root systems capturing sufficient nutrients. Typically, vegetative growth is extended, allowing resource accumulation and investment in seed production. In environments where these nutrients are limiting, overall growth is reduced but root systems are expanded and colonization by microorganisms is encouraged to facilitate nutrient capture. Plants can recognize a patchwork of nutrient availability and activate root growth within this patchwork to optimize nutrient capture.

Plants are able to measure multiple facets of nutrient availability: local sensing of nutrients in the soil, roots experiencing nutrient deprivation, roots experiencing high nutrient availability, and the total nutrient requirements of the plant. Such sensing involves an integration of root and shoot signaling, with a variety of hormones moving between the root and the shoot to both signal nutrient availability and coordinate plant development. Such root-shoot-root signaling is essential to allow plants to make use of local nutrient patches, but to do so only when there is sufficient need for that nutrient.

Some microorganisms have capabilities for the capture of N and P from the environment. For instance, N-fixing bacteria can access nitrogen from the atmosphere, something that plants are unable to do. Arbuscular mycorrhizal fungi can access insoluble forms of phosphate in the soil that are mostly inaccessible to plants. Under situations where plants are unable to access N and P from their immediate environment, they turn to these microorganisms to find new sources of these limiting nutrients. Many of the processes that coordinate the plants’ developmental response to nutrient availability also regulate the plants’ interaction with microorganisms. These processes regulate the plants’ receptiveness to their microbial communities, promoting symbiotic associations and restricting immunogenic processes.

OUTLOOK

Although our understanding of how plants engage with nutrients has advanced, there are few examples of how such knowledge has affected plant performance, perhaps because much of our understanding derives from studies in model, not crop, plants. Years of breeding crops for success under high-nutrient environments have left us with some crop varieties that are poor at optimizing use of limited nutrients. Nonetheless, many processes exist in plants to ensure productivity under poor nutrient conditions, some of which are already accessible in the diversity of crop species and wild near-relatives. We are poised to use the knowledge generated in model systems to optimize the performance of crop plants under nutrient limitation.

N response and signaling.

Root responses of Arabidopsis plants grown in uniform high N (NO3; dark gray, left), uniform low N (light gray, middle), and differential treatments of high and low N (right). Note how the root responses are opposite to the local treatments in uniform versus differential treatments. Underpinning these responses are C-terminally encoded peptides (CEPs) produced in roots experiencing low N, cytokinins produced in roots experiencing high N, and an N-sufficiency signal in the shoot. All regulate shoot-to-root signaling, which involves CEP DOWNSTREAM 1 (CEPD) peptides. Systemic signaling is integrated with local signaling (indicated by red) that is induced by local perception of NO3.

Abstract

As primary producers, plants rely on a large aboveground surface area to collect carbon dioxide and sunlight and a large underground surface area to collect the water and mineral nutrients needed to support their growth and development. Accessibility of the essential nutrients nitrogen (N) and phosphorus (P) in the soil is affected by many factors that create a variable spatiotemporal landscape of their availability both at the local and global scale. Plants optimize uptake of the N and P available through modifications to their growth and development and engagement with microorganisms that facilitate their capture. The sensing of these nutrients, as well as the perception of overall nutrient status, shapes the plant’s response to its nutrient environment, coordinating its development with microbial engagement to optimize N and P capture and regulate overall plant growth.

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