Ethylene and Phloem Signals Are Involved in the Regulation of Responses to Fe and P Deficiencies in Roots of Strategy I Plants

Abstract

Iron (Fe) and phosphorus (P) are two essential mineral nutrients whose acquisition by plants presents important environmental and economic implications. Both elements are abundant in most soils but scarcely available to plants. To prevent Fe or P deficiency dicot plants initiate morphological and physiological responses in their roots aimed to specifically acquire these elements. The existence of common signals in Fe and P deficiency pathways suggests the signaling factors must act in conjunction with distinct nutrient-specific signals in order to confer tolerance to each deficiency. Previous works have shown the existence of cross talk between responses to Fe and P deficiency, but details of the associated signaling pathways remain unclear. Herein, the impact of foliar application of either P or Fe on P and Fe responses was studied in P- or Fe-deficient plants of Arabidopsis thaliana, including mutants exhibiting altered Fe or P homeostasis. Ferric reductase and acid phosphatase activities in roots were determined as well as the expression of genes related to P and Fe acquisition. The results obtained showed that Fe deficiency induces the expression of P acquisition genes and phosphatase activity, whereas P deficiency induces the expression of Fe acquisition genes and ferric reductase activity, although only transitorily. Importantly, these responses were reversed upon foliar application of either Fe or P on nutrient-starved plants. Taken together, the results reveal interactions between P- and Fe-related phloem signals originating in the shoots that likely interact with hormones in the roots to initiate adaptive mechanisms to tolerate deficiency of each nutrient.

Nitrogen and Phosphorus Interplay in Lupin Root Nodules and Cluster Roots

“…Organic anion secretion and rhizosphere acidification mobilize not only P but also other nutrients like Fe, Ca, Mn, or Zn, increasing their uptake rates (Lamont, 2003). P is loaded into the xylem through transporters (Lucena et al, 2019). Phosphorus deficiency initially reduces the levels of sugars (fructose, glucose, and sucrose) in shoots, and phosphorylated metabolites such as glycerol-3-phosphate, fructose-6-phosphate, glucose-6-phosphate, or myo-inositol-phosphate levels decrease in both shoots and roots of L. albus (Müller et al, 2015).…”

“…Organic anion secretion and rhizosphere acidification mobilize not only P but also other nutrients like Fe, Ca, Mn, or Zn, increasing their uptake rates ( Lamont, 2003 ). P is loaded into the xylem through transporters ( Lucena et al, 2019 ).…”

“…Recently, miR399 has also been linked to legume nodule functional processes ( Figueredo et al, 2020 ). The importance of ethylene and miR399 has been reported in the regulation of responses to Fe and P deficiencies ( Lucena et al, 2019 ). Nitric oxide (NO) is another signaling molecule related to both N and P signaling.…”

Influence of Ethylene Signaling in the Crosstalk Between Fe, S, and P Deficiency Responses in Arabidopsis thaliana

“…Among these responses are the enhanced expression of specific transporters and the alteration of the root system architecture (Maruyama-Nakashita et al, 2006 ; Takahashi et al, 2011 ; Zhang et al, 2014 ; Briat et al, 2015b ; García et al, 2015 ; Lucena et al, 2015 ; Ajmera et al, 2019 ; Crombez et al, 2019 ; Venuti et al, 2019 ). In Arabidopsis , the main phosphate transporters implicated in its acquisition from the medium are PHT1;1 and PHT1;4 (also named PT1 and PT2; Nagarajan and Smith, 2012 ; Lucena et al, 2018 , 2019 ; Crombez et al, 2019 ); the ones for sulfate are SULTR1;1 and SULTR1;2 (Maruyama-Nakashita et al, 2006 ; Takahashi et al, 2011 ; Yamaguchi et al, 2020 ), and the one for Fe 2+ is IRT1 (Kobayashi and Nishizawa, 2012 ; Lucena et al, 2015 ). Nutrient deficiencies also alter the expression of internal transporters, like PHT1;5, which plays a critical role in mobilizing phosphate from source to sink organs (Nagarajan et al, 2011 ; Nagarajan and Smith, 2012 ; Zhang et al, 2014 ).…”

“…Both Fe and P deficiencies can induce other responses, like the acidification of the rhizosphere; the increased synthesis and release of organic acids and phenolics to the rhizosphere; and the development of subapical root hairs (Kobayashi and Nishizawa, 2012 ; Correia et al, 2014 ; Wang et al, 2014 ; Zhang et al, 2014 ; García et al, 2015 ; Lucena et al, 2015 , 2018 , 2019 ; Neumann, 2016 ; Tsai and Schmidt, 2017 ; Venuti et al, 2019 ). Particularly, Fe deficiency can induce an enhanced ferric reductase activity (FRA), due to increased expression of the FRO2 gene (Kobayashi and Nishizawa, 2012 ; Lucena et al, 2015 ), and P deficiency an enhanced phosphatase activity (PA), due to increased expression of PAP genes, like PAP7 or PAP17 (also named ACP5 ; Lei et al, 2011 ; Zhang et al, 2014 ; Lucena et al, 2018 , 2019 ; Venuti et al, 2019 ).…”