Nitrogen and Phosphorus Interplay in Lupin Root Nodules and Cluster Roots

Abstract

Nitrogen (N) and phosphorus (P) are two major plant nutrients, and their deficiencies often limit plant growth and crop yield. The uptakes of N or P affect each other, and consequently, understanding N–P interactions is fundamental. Their signaling mechanisms have been studied mostly separately, and integrating N–P interactive regulation is becoming the aim of some recent works. Lupins are singular plants, as, under N and P deficiencies, they are capable to develop new organs, the N2-fixing symbiotic nodules, and some species can also transform their root architecture to form cluster roots, hundreds of short rootlets that alter their metabolism to induce a high-affinity P transport system and enhance synthesis and secretion of organic acids, flavonoids, proteases, acid phosphatases, and proton efflux. These modifications lead to mobilization in the soil of, otherwise unavailable, P. White lupin (Lupinus albus) represents a model plant to study cluster roots and for understanding plant acclimation to nutrient deficiency. It tolerates simultaneous P and N deficiencies and also enhances uptake of additional nutrients. Here, we present the structural and functional modifications that occur in conditions of P and N deficiencies and lead to the organogenesis and altered metabolism of nodules and cluster roots. Some known N and P signaling mechanisms include different factors, including phytohormones and miRNAs. The combination of the individual N and P mechanisms uncovers interactive regulation pathways that concur in nodules and cluster roots. L. albus interlinks N and P recycling processes both in the plant itself and in nature.

Interaction Between Macro‐ and Micro-Nutrients in Plants

“…More importantly, the effect of N-deficiency is less important for plants under P-deficiency. Recently, Pueyo et al (2021) reported structural and functional modifications in roots, leading to the formation of clusters and altered FIGURE 1 | Schematic representation of nitrogen-starvation response and phosphate-starvation responses explaining N/P interactions. PHR1 acts as a major transcriptional regulator of P-starvation response, which is accompanied by the activation of phosphate starvation-induced (PSI) genes followed by phosphate uptake and translocation by phosphate transporters (PHO1 and PHT1s).…”

“…More importantly, the effect of N-deficiency is less important for plants under P-deficiency. Recently, Pueyo et al (2021) reported structural and functional modifications in roots, leading to the formation of clusters and altered nodule metabolism, under P and N deficiencies. Signaling factors, including phytohormones and miRNAs, were reported to be the important players in the N and P interactions.…”

“…Based on the available reports and nutritional interactions, it can be concluded that PHR1 and HY5 act as master regulators of multiple nutrient homeostasis. Moreover, the role of miRNAs as a potential regulator of the cross-talks between the nutrient homeostasis is also being deciphered ( Hsieh et al, 2009 ; Pant et al, 2009 ; Liang et al, 2015 ; Pueyo et al, 2021 ). The involvement of epigenetic and epitranscriptomic marks ( Wang et al, 2016 ; Kumar et al, 2018 ; Kumar and Mohapatra, 2021 ) in regulating nutrient interactions is yet to be explored.…”

Editorial: Nutrient Interactions in Plants

“…Regarding the reviews; one is related to interactions between two essential elements, S and Fe (Astolfi et al, 2021); two are related to interactions between macro-and micro-nutrients (Fan et al, 2021;Kumar et al, 2021); and the other two are dedicated to interactions between beneficial elements, Si and Se, and essential ones (Pavlovic et al, 2021;Zhou et al). The minireview deals with the interaction between N and P in the development of root nodules and cluster roots (Pueyo et al, 2021). The perspective article is devoted to describing new approaches based on computational analysis to predict interactions between proteins related to different elements (Di Silvestre et al).…”

Nodulated White Lupin Plants Growing in Contaminated Soils Accumulate Unusually High Mercury Concentrations in Their Nodules, Roots and Especially Cluster Roots

“…This increase in root exudation surface enhances nutrient mobilization in the rhizosphere [26,30]. Nodules and cluster roots have major roles in lupin N and P metabolisms, respectively, but there are interactive regulation pathways between both organs that interlink N and P recycling [33].…”