A Shoot Fe Signaling Pathway Requiring the OPT3 Transporter Controls GSNO Reductase and Ethylene in Arabidopsis thaliana Roots

Abstract

Ethylene, nitric oxide (NO) and glutathione (GSH) increase in Fe-deficient roots of Strategy I species where they participate in the up-regulation of Fe acquisition genes. However, S-nitrosoglutathione (GSNO), derived from NO and GSH, decreases in Fe-deficient roots. GSNO content is regulated by the GSNO-degrading enzyme S-nitrosoglutathione reductase (GSNOR). On the other hand, there are several results showing that the regulation of Fe acquisition genes does not solely depend on hormones and signaling molecules (such as ethylene or NO), which would act as activators, but also on the internal Fe content of plants, which would act as a repressor. Moreover, different results suggest that total Fe in roots is not the repressor of Fe acquisition genes, but rather the repressor is a Fe signal that moves from shoots to roots through the phloem [hereafter named LOng Distance Iron Signal (LODIS)]. To look further in the possible interactions between LODIS, ethylene and GSNOR, we compared Arabidopsis WT Columbia and LODIS-deficient mutant opt3-2 plants subjected to different Fe treatments that alter LODIS content. The opt3-2 mutant is impaired in the loading of shoot Fe into the phloem and presents constitutive expression of Fe acquisition genes. In roots of both Columbia and opt3-2 plants we determined 1-aminocyclopropane-1-carboxylic acid (ACC, ethylene precursor), expression of ethylene synthesis and signaling genes, and GSNOR expression and activity. The results obtained showed that both ‘ethylene’ (ACC and the expression of ethylene synthesis and signaling genes) and ‘GSNOR’ (expression and activity) increased in Fe-deficient WT Columbia roots. Additionally, Fe-sufficient opt3-2 roots had higher ‘ethylene’ and ‘GSNOR’ than Fe-sufficient WT Columbia roots. The increase of both ‘ethylene’ and ‘GSNOR’ was not related to the total root Fe content but to the absence of a Fe shoot signal (LODIS), and was associated with the up-regulation of Fe acquisition genes. The possible relationship between GSNOR(GSNO) and ethylene is discussed.

Assessment of Subcellular ROS and NO Metabolism in Higher Plants: Multifunctional Signaling Molecules

“…NO also preserves Fe homeostasis through crosstalk with ethylene and auxin phytohormones, ferritin and frataxin and through its ability to form nitrosyl iron complexes [162]. New elements, such as GSH, GSNO, and GSNO reductase, have been found in the complex relationships with the Long distance iron signal which moves from shoots to roots through the phloem to regulate Fe homeostasis [163]. GSNOR activity, in particular, has been found necessary for Fe homeostasis, especially under Fe-toxicity conditions in roots [164].…”

Gasotransmitters in Action: Nitric Oxide-Ethylene Crosstalk during Plant Growth and Abiotic Stress Responses

“…Recently, this model was supplemented by the regulatory role of GSNO and GSNOR in Fe-deficient roots. ET (ACC) was found to increase GSNOR activity and expression leading to low GSNO level which, through unblocking ET synthesis, can maintain ET production in Fe-deficient roots [159].…”

Small-Molecules Selectively Modulate Iron-Deficiency Signaling Networks in Arabidopsis

“…Under Fe starvation, a wide range of chemical signals coordinate and trigger the transcriptional response (Liu et al, 2016). Some studies have suggested that cellular Fe, especially the levels in leaf vasculature itself act as a sensing/signaling component (Kumar et al, 2017; Garcia et al, 2018; Khan et al, 2018). Based on these findings, together with action of R3 and R7, it is clear that multilayered signaling networks exist.…”

“…Based on these findings, together with action of R3 and R7, it is clear that multilayered signaling networks exist. Importantly, there is lot of interconnection and feed-/forward-back between these signaling molecules, that influence each other, levels and activity under Fe-starvation (Garcia et al, 2011, 2018; Brumbarova et al, 2015; Liu et al, 2016). Therefore, further study of R3 may reveal the identity of a hidden unknown novel component that regulates the central transcription factor FIT.…”

“…Many molecules/metabolites such as sucrose, putrescine, nitric oxide (NO) and S -nitrosoglutathione (GSNO), and the hormones auxin and ethylene participate in the signaling process and positively regulate Fe-deficiency transcription (Chen et al, 2010; Lin et al, 2015; Lucena et al, 2015; Liu et al, 2016; Zhu et al, 2016; Kailasam et al, 2018); whereas the hormones, cytokinin, abscisic acid (ABA) and jasmonic acid (JA) act negatively on the network (Liu et al, 2016; Cui et al, 2018). A recent study by Garcia et al (2018) discussed the different signaling modes, in the form LODIS (LOng Distance Iron Signal) or LODIS-derived and also via NO/GSNO, to the transcription factors. We previously undertook a chemical screening and dissected the Fe-signaling pathway using a small-molecule named R7 (Kailasam et al, 2018).…”