Natural variation for Fe-efficiency is associated with upregulation of Strategy I mechanisms and enhanced citrate and ethylene synthesis in Pisum sativum L.

Abstract

Iron (Fe)-deficiency is a common abiotic stress in Pisum sativum L. grown in many parts of the world. The aim of the study was to investigate variation in tolerance to Fe deficiency in two pea genotypes, Santi (Fe-efficient) and Parafield (Fe-inefficient). Fe deficiency caused greater declines in chlorophyll score, leaf Fe concentration and root-shoot development in Parafield compared to Santi, suggesting greater Fe-efficiency in Santi. Fe chelate reductase activity and ethylene production were increased in the roots of Santi and to a lesser extent in Parafield under Fe deficiency, while proton extrusion was only occurred in Santi. Moreover, expression of the Fe chelate reductase gene, FRO1, and Fe transporter, RIT1 were upregulated in Fe-deficient roots of Santi. Expression of HA1 (proton extrusion) was also significantly higher in Santi when compared to Parafield grown in Fe-deficient conditions. Furthermore, the application of the ethylene biosynthesis inhibitor, 1-aminoisobutyric acid reduced the Fe chelate reductase activity, supporting a direct role for ethylene in its induction. A significant increase in root citrate was only observed in Santi under Fe deficiency indicating a role for citrate in the Fe-efficiency mechanism. Taken together, our physiological and molecular data indicate that genotypic variation in tolerance to Fe deficiency in Santi and Parafield plants is a result of variation in a number of Strategy I mechanisms and also suggest a direct role for ethylene in Fe reductase activity. The pea cultivar, Santi provides a new source of Fe-efficiency that can be exploited to breed more Fe-efficient peas.

The Understanding of the Plant Iron Deficiency Responses in Strategy I Plants and the Role of Ethylene in This Process by Omic Approaches

“…For example, it has been reported that the expression of FRO2 and IRT1 is positively or negatively affected by several hormones, such as auxin, ethylene, cytokinins, jasmonic acid, and brassinosteroids, and other signaling molecules, including nitric oxide (Hindt and Guerinot, 2012; Kobayashi and Nishizawa, 2012). Among them, ethylene has been extensively explored in the involvement of Fe deficiency response by application of ethylene precursors or inhibitors or ethylene related mutants (Romera and Alcantara, 1994; Schmidt et al, 2000; Schikora and Schmidt, 2001, 2002; Schmidt and Schikora, 2001; Zaid et al, 2003; Lucena et al, 2006; Waters et al, 2007; Garcia et al, 2010, 2011; Wu et al, 2011; Kabir et al, 2012; Garcia et al, 2015; Ye et al, 2015). It has been uncovered (Lingam et al, 2011) that ethylene regulates the expression of Fe acquisition genes via modulation of FIT protein stability through the interaction between FIT and ETHYLENE INSENSITIVE3 (EIN3)/ETHYLENE INSENSITIVE3-LIKE1 (EIL1).…”

SNP marker discovery, linkage map construction and identification of QTLs for enhanced salinity tolerance in field pea (Pisum sativumL.)

“…In combination, these factors can cause nutrient (Fe, K) deficiencies and soil toxicities (such as to elevated levels of boron) that limit growth and grain yield potential. For field pea, relatively high and heritable genetic tolerances to Fe deficiency [29] and boron toxicity [30-32] have been identified. In terms of salinity tolerance, preliminary studies based on biomass reduction indicated that field pea is significantly more sensitive than other commonly cultivated Australian broad-acre crops such as barley [33,34], wheat [35] and canola [36], due to a low salinity threshold level [37] in pea.…”

Mechanisms associated with Fe‐deficiency tolerance and signaling in shoots of Pisum sativum

“…Responses may confer better Fe acquisition and transport, enhancing tolerance of low Fe in soil; however for simplicity, all these mechanisms are referred to here as deficiency tolerance. Responses induced in strategy I plants (dicots and non‐graminaceous monocots) are increased Fe‐reductase activity, proton extrusion and citrate and ethylene production in roots (Schmidt , Waters et al , Curie and Briat , López‐Millán et al 2001, Kabir et al ). The strategy II response (unique to the Graminaceae) relies on the secretion of phytosideropores (PS) into the rhizosphere which rapidly chelate Fe(III) to form Fe(III)‐PS chelates that are subsequently transported into root cells through specific transporters (Curie and Briat ).…”