Reappraisal of the central role of soil nutrient availability in nutrient management in light of recent advances in plant nutrition at crop and molecular levels

https://doi.org/10.1016/j.eja.2020.126069Get rights and content

Abstract

The concept of soil nutrient availability is still widely viewed within the framework of crop yield responses to fertilizer applications as the intermediary variable linking the rate of application of a single nutrient to the absorption of this nutrient by plants according to the pioneer work of Boussingault (1855), von Liebig (1855), and Mitscherlich (1924). For interpreting the huge variability of crop yield responses to increasing fertilizer applications, agronomists and soil scientists have focused on soil nutrient dynamics in order to estimate the quantity of each nutrient available for plant uptake. This linear approach considering “available nutrient in soil” as an external factor to which plants respond does not correspond to the reality for three main reasons: (i) the root absorption capacity is deeply feed-back controlled by the plant growth capacity itself and, therefore, does not depend univocally on soil nutrient availability; (ii) interactions among different nutrients in soils and plants imply that the availability of one nutrient for plants depends of the availability of others, requiring a more integrated approach; and (iii) the plant itself influences nutrient dynamic processes in soils through interactions with microbial communities in its rhizosphere. Consequently, soil nutrient availability cannot be only considered as a property of the external medium to which plants adapt, but also, and more importantly, as resulting of the functioning of the whole plant-soil-living organisms ecosystem. This review paper proposes an integrated and hypothesis-based vision of plant mineral nutrition based on several recent findings: (i) the corroboration and verification of hypotheses of regulation of plant nutrient uptake at the whole plant level by recent advances in the molecular physiology of plant nutrition, (ii) the physiological basis for interactions among different plant nutrients, and (iii) the increasing evidence of plant-soil interactions at the rhizosphere level.

Introduction

Plant mineral nutrition research has been dominated during the last two centuries by agronomists dealing with the determination of optimum fertilizer applications to crops to achieve the maximum yield potentially determined by climate and genotype. Jean-Baptiste Boussingault (1855) first identified the role of nitrate as the main source for the nitrogen (N) nutrition of plants. Justus von Liebig (1855) then established the Law of the Minimum: “plants grow only to the extent allowed by the single nutrient that is most limiting” and, later on, Mitscherlich (1924) established the Law of Diminishing Return in which the crop response to the addition of one nutrient decreases as the level of application increases. All these paradigms constituted the basis for plant nutrition and crop fertilization management around the world as soon as external fertilizer resources became available for agriculture through the industrial Haber-Bosh process for the production of N fertilizers and the mining industry for the production of phosphorus (P) and potassium (K) fertilizers.

Crop mineral nutrition has long been studied by empirical “rate-response” approaches linking the rate of fertilizer application with crop yield. For a better understanding of these rate-response curves, the concept of “soil nutrient availability” for plants was proposed in order to separate the whole effect of fertilization into: (i) the effect of application rates on soil nutrient availability and (ii) the effect of increasing soil nutrient availability on crop yield (de Wit, 1994). Soil nutrient availability was then considered as the pivotal variable and as an external factor to which plants respond. This approach has been dominated by soil physico-chemistry focusing on the interaction between the different nutrient elements and the soil mineral matrix for the determination of the “nutrient availability”. Plant physiologists were then left with dealing with the relationship between “nutrient availability” and root absorption processes.

Over the last 30 years, studies on the dynamics of plant and crop nutrition (see recent review of Lemaire et al., 2019) based on allometry between nutrient uptake (N, P, and K) and above ground biomass accumulation by crops have resulted in a more integrated hypothesis of crop nutrient uptake in which the rate of nutrient uptake by plants is co-regulated by both the nutrient concentration in the root medium and the plant growth capacity itself (Devienne-Baret et al., 2000). This co-regulation of nutrient absorption has been experimentally established as a long distance signaling from shoots to roots (Ismande and Touraine (1994); Tourraine et al., 1994; Forde, 2002). So, if such a co-regulation occurs, it implies that “nutrient availability in soil” cannot be longer considered only as an external factor for plants, but as resulting also of the functioning of the integrated soil-plant system. Moreover, the analysis of interactions between the different nutrient elements (N, P, and K) as allowed by this approach indicates clearly that the availability of one given element for plants is in large part determined by the availability of other elements (see Lemaire et al., 2019), leading then to strong interactions between the different nutrients.

Research in plant physiology for understanding plant N mineral nutrition and the regulation of nutrient absorption processes by roots have been conducted by using very simplified experimental systems, such as excised roots or young germinating seedlings. This approach allowed a precise characterization of the kinetics of in planta nutrient transport systems, that is to say the function describing their instantaneous transport activity over a range of external nutrient concentrations. In such a system, the availability of nutrient was considered an external factor for plants, which allowed a quantitative analysis of absorption in response to variations in nutrient concentration within the root medium (Rao and Rains, 1976). Although convenient for fast laboratory experiments, these experimental systems did not allow the unravelling of the regulatory mechanisms controlling the transport systems in intact autotrophic plants. More recently, molecular approaches allowed the identification of the different root membrane transporter proteins for the absorption of nitrate and ammonium, and of P, K, and other mineral elements (Nacry et al., 2013) and demonstrated that the expression of genes coding these proteins were feed-back regulated by plant shoot signals (Gansel et al., 2001; Chen et al., 2016; Ohkubo et al., 2017).

In parallel with these advances in plant physiology, research in soil science progressed in the understanding of soil-plant-microbe interactions by going beyond the restricted physico-chemistry and static vision of soil nutrient availability. Tremendous progress has been made recently thanks to the dynamic analysis of the soil microbiome under various nutrition conditions (Stringlis et al., 2018), through the analysis of root exsudates for solubilization of different minerals (Voges et al., 2019; Dakora and Phillips, 2002; Sisó-Terraza et al., 2016), and the role of soil microbe communities for providing available nutrients to plants (Jacoby et al., 2017; Garcia and Kao-Kniffin, 2018). Plants and microbes associated within the rhizosphere are playing an important role in the availability of N, P, K and other nutrients for root absorption.

The overall objective of this review paper is to develop an integrated and hypothesis-based vision of plant mineral nutrition. More specifically, we wanted (i) to demonstrate how these different hypotheses of regulation at the whole plant-soil system are corroborated and verified by recent advances in the molecular physiology analysis of the different processes involved in plant nutrition, (ii) to present new evidence of the physiological basis for analyzing interactions among different plant nutrients, and (iii) to analyze the plant-soil interactions at the rhizosphere level for a more integrated view of the soil-plant-microbe system.

Section snippets

Evidence for a co-regulation of N absorption by both soil N availability and plant growth dynamics

Empirical studies demonstrated clearly that N uptake dynamics by different forage crop species is strongly controlled by aboveground plant mass accumulation (Lemaire and Salette, 1984a, b; Lemaire et al., 1985). As represented in Fig. 1, the large variation in N uptake (N) by perennial grasslands due to years, species, and genotypes is fully explained by the differences in the dynamics of aboveground biomass accumulation (W).

Greenwood et al. (1990); Lemaire and Gastal (1997), and Gastal and

Molecular control of plant N absorption dynamics

The past 20 years have seen a tremendous breakthrough in our understanding of the mechanisms governing N acquisition by plants. This occurred first in the model species Arabidopsis thaliana, where molecular studies of N uptake systems provided a strong support to the hypothesis of co-regulation of root N uptake by both external N availability and the plant growth dynamics (see section 1.1).

How root-microbes interactions control soil nutrient availability for plants?

Plant mineral uptake is feed-back controlled by plant growth, as reported above. Nevertheless, this uptake heavily depends on the physico-chemical properties of the soil mineral matrix, which determine the equilibrium among different mineral forms more or less usable by plants (see Fig. 5B). In addition to soil physico-chemical properties, the actual mineral availability for plants, representing the pool of minerals that will be taken up by the plants, either directly through root cells and/or

Conclusion

The estimation of soil nutrient availability, as resulting only from the fertilizer supply and soil attributes and expressed either as a stock or as a concentration, is not sufficient for determining alone plant nutrient uptake dynamics and for the prognosis of crop yield responses to fertilizer applications. Several reasons for a more systemic approach have been proposed: (i) plants are a key driver of the soil nutrient availability through the auto-regulation of their own capacity for

Authors contributions

J.F. Briat, conceptualization of the whole paper and co-writing §4. A. Gojon: conceptualization and writing §2. C. Plassard: conceptualization and co-writing §4. H. Rouached: conceptualization and writing §3. G. Lemaire: conceptualization and coordination of the whole paper, writing §2.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We wish to acknowledge Dr. Gilles Bélanger for his numerous suggestions, and careful English editing, which contributed to deeply improve this manuscript. This paper originates from an academic session at the "Académie d'Agriculture de France" which took place in Paris, April 19, 2019 (https://www.academie-agriculture.fr/actualites/academie/seance/academie/approches-systemiques-de-la-nutrition-minerale-des-plantes-en)

References (98)

  • A.G. Assunção et al.

    Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency

    Proc. Natl. Acad. Sci. U. S. A.

    (2010)
  • H.P. Bais et al.

    The role of root exudates in rhizosphere interactions with plants and other organisms

    Annu. Rev. Plant Biol.

    (2006)
  • N. Bouain et al.

    Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation

    PLoS Genet.

    (2019)
  • J.B. Boussingault

    Recherches sur la végétation. De l’action du salpêtre sur le développement des plantes

    J. Pharm. Chimie

    (1855)
  • J.F. Briat et al.

    Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of phosphate starvation response 1 (PHR1)

    Front. Plant Sci.

    (2015)
  • M.C. Brundrett et al.

    Evolutionary history of mycorrhizal symbioses and global host plant diversity

    New Phytol.

    (2018)
  • P. Buchner et al.

    Complex phylogeny and gene expression patterns of the members of the nitrate transporter1/peptide transporter family (NPF) in wheat

    J. Exp. Bot.

    (2014)
  • D. Bulgarelli et al.

    Structure and functions of the bacterial microbiota of plants

    Annu. Rev. Plant Biol.

    (2013)
  • M. Caloin et al.

    Analysis of the time course change in nitrogen content of Dactylis glomerata L. Using a model of plant growth

    Ann. Bot.

    (1984)
  • R. Chutia et al.

    Iron and phosphate deficiency regulators concertedly control coumarin profiles in Arabidopsis thaliana roots during iron, phosphate, and combined deficiencies

    Front. Plant Sci.

    (2019)
  • M. Clarholm

    Bacteria and protozoa as integral components of the forest ecosystem – their role in creating a naturally varied soil fertility

    Antonie Van Leeuwenhoek

    (2002)
  • A. Corrêa et al.

    Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown

    Mycorrhiza

    (2015)
  • F.D. Dakora et al.

    Root exudates as mediators of mineral acquisition in low-nutrient environments

    Plant Soil

    (2002)
  • C.T. De Wit

    Resource use analysis in agriculture: a struggle for interdisciplinarity

  • P. Delhon et al.

    Diurnal regulation of NO3 uptake in soybean plants. IV. Dependence on current photosynthesis and sugar availability to the roots

    J. Exp. Bot.

    (1996)
  • F. Devienne-Baret et al.

    Integrated control of nitrate uptake by crop growth rate and soil nitrate availability under field conditions

    Ann. Bot.

    (2000)
  • M. Duru et al.

    A nitrogen and phosphorus herbage nutrient index as a tool for assessing the effect of N and P supply on the dry matter yield of permanent pastures

    Nutr. Cycl. Agroecosyst.

    (1997)
  • M. Duru et al.

    N and P-K status of herbage: use for diagnosis of grasslands

  • Facelli et al.

    Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition

    New Phytol.

    (2010)
  • B.G. Forde

    The role of long-distance signaling in plant response to nitrate and other nutrients

    J. Exp. Bot.

    (2002)
  • P. Fourcroy et al.

    Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency

    New Phytol.

    (2014)
  • X. Gansel et al.

    Differential regulation of the NO3 and NH4+ transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant

    Plant J.

    (2001)
  • J. Garcia et al.

    Microbial group dynamics in plant rhizospheres and their implications on nutrient cycling

    Front. Microbiol.

    (2018)
  • T. Garnett et al.

    The response of the maize nitrate transport system to nitrogen demand and supply across the lifecycle

    New Phytol.

    (2013)
  • F. Gastal et al.

    N uptake and distribution in crops: an agronomical and ecophysiological perspective

    J. Exp. Bot.

    (2002)
  • F. Gastal et al.

    Relationships between nitrogen uptake and carbon assimilation in whole plant of tall fescue

    Plant Cell Environ.

    (1989)
  • A. Gojon et al.

    Nitrate transceptor(s) in plants

    J. Exp. Bot.

    (2011)
  • D.J. Greenwood et al.

    Decline in percentage N of C3 and C4 crops with increasing plant mass

    Ann. Bot.

    (1990)
  • B.S. Griffiths

    Soil nutrient flow

    Soil Protozoa

    (1994)
  • M. Guether et al.

    A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi

    Plant Physiol.

    (2009)
  • S. Hara et al.

    Isolation of inositol hexaphosphate (IHP)-degrading bacteria from arbuscular mycorrhizal fungal hyphal compartments using a modified baiting method involving alginate beads containing IHP

    Microbes Environ.

    (2016)
  • M.J. Harrison et al.

    A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi

    Plant Cell

    (2002)
  • J.D. Hoeksema et al.

    A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi

    Ecology Lett.

    (2010)
  • B. Hu et al.

    Nitrate–NRT1. 1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants

    Nat. Plants

    (2019)
  • U. Irshad et al.

    Phosphorus acquisition from phytate depends on efficient bacterial grazing, irrespective of the mycorrhizal status of Pinus pinaster

    Plant Soil

    (2012)
  • J. Ismande et al.

    N demand and regulation of nitrate uptake

    Plant Physiol.

    (1994)
  • R. Jacoby et al.

    The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions

    Front. Plant Sci.

    (2017)
  • I. Jakobsen et al.

    Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores

    New Phytol.

    (2001)
  • G.A. Khan et al.

    Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1; H3 in Arabidopsis

    J. Exp. Bot.

    (2014)
  • Cited by (53)

    View all citing articles on Scopus
    View full text