Water impacts nutrient dose responses genome-wide to affect crop production

Abstract

Changes in nutrient dose have dramatic effects on gene expression and development. One outstanding question is whether organisms respond to changes in absolute nutrient amount (moles) vs. its concentration in water (molarity). This question is particularly relevant to plants, as soil drying can alter nutrient concentration, without changing its absolute amount. To compare the effects of amount vs. concentration, we expose rice to a factorial matrix varying the dose of nitrogen (N) and water (W) over a range of combinations, and quantify transcriptome and phenotype responses. Using linear models, we identify distinct dose responses to either N-moles, W-volume, N-molarity (N/W), or their synergistic interaction (N×W). Importantly, genes whose expression patterns are best explained by N-dose and W interactions (N/W or N×W) in seedlings are associated with crop outcomes in replicated field trials. Such N-by-W responsive genes may assist future efforts to develop crops resilient to increasingly arid, low nutrient soils.

A balancing act: how plants integrate nitrogen and water signals

“…Over the past decade, transcriptomic approaches have been employed to investigate how plants signal changes in N or W availability at the molecular level. These studies have revealed that thousands of genes are differentially expressed in response to either changes in N dose or W status, highlighting that the gene regulatory networks that govern responses to N and W are highly complex ( Vidal and Gutierrez, 2008 ; Wilkins et al , 2010 ; Sharma et al , 2018 ; Swift et al , 2019 ).…”

“…Indeed, given their central role in plant physiology, N and W have many combinatorial effects on plant phenotypes. Arguably the most important interaction is their combined effect on biomass and crop yield potential—which is only achieved when both N and W are non-limiting ( Patterson et al , 1997 ; Di Paolo and Rinaldi, 2008 ; Brueck and Senbayram, 2009 ; Shi et al , 2014 ; Swift et al , 2019 ) ( Fig. 1A ).…”

“… N and W doses combine to impact plant physiology and gene regulation. (A) (A.1) N and W combine to have a synergistic interaction on shoot biomass in rice ( Swift et al , 2019 ). (A.2) A single integrated study of N and W dose responses performed in rice reveals plant responses to N dose as (moles) or N concentration (N/W), which exhibit distinct transcriptomic responses.…”

“…(A.2) A single integrated study of N and W dose responses performed in rice reveals plant responses to N dose as (moles) or N concentration (N/W), which exhibit distinct transcriptomic responses. Additionally, the dose of N and W also exhibits a synergistic effect (N×W) on gene expression responses and phenotypes ( Swift et al , 2019 ). (A.3) Stomatal opening and transpiration are influenced by N and W availability ( Shi et al , 2014 ).…”

Nutrient dose-responsive transcriptome changes driven by Michaelis–Menten kinetics underlie plant growth rates

“…Indeed, previous studies have shown that N nutrient dose sensing enables plants to reprogram both their gene expression patterns (8,9) as well as their phenotype, including the rate of N uptake and plant growth (10,11). However, what remains unknown are the molecular mechanisms that enable the dose of N to inform gene expression levels, and how such gene expression changes lead to dose-responsive changes in plant phenotype.…”