Ethylene and the Regulation of Physiological and Morphological Responses to Nutrient Deficiencies

Abstract

To cope with nutrient deficiencies, plants develop both morphological and physiological responses. The regulation of these responses is not totally understood, but some hormones and signaling substances have been implicated. It was suggested several years ago that ethylene participates in the regulation of responses to iron and phosphorous deficiency. More recently, its role has been extended to other deficiencies, such as potassium, sulfur, and others. The role of ethylene in so many deficiencies suggests that, to confer specificity to the different responses, it should act through different transduction pathways and/or in conjunction with other signals. In this update, the data supporting a role for ethylene in the regulation of responses to different nutrient deficiencies will be reviewed. In addition, the results suggesting the action of ethylene through different transduction pathways and its interaction with other hormones and signaling substances will be discussed.

Figure 1.

Ethylene generally acts as an activator of responses to nutrient deficiencies. Consequently, ethylene inhibitors block these responses. As an example, ferric reductase activity is enhanced under Fe deficiency (denoted by the purple color of the assay solution) but blocked upon application of the ethylene inhibitor STS. Tomato plants grown in complete nutrient solution (+Fe) were transferred for the last 3 d to nutrient solution either without Fe (−Fe) or without Fe plus 400 μm STS (−Fe + STS). Ferric reductase activity was determined as described by Romera and Alcántara (1994).

Figure 2.

Effect of P deficiency on AtPT2 gene expression (A) and Fe deficiency on ferric reductase activity (B) in Arabidopsis wild-type (WT) Columbia-0 plants and ethylene mutants (ctr1, ethylene-constitutive mutant; ein2, ethylene-insensitive mutant; eto1, ethylene overproducer mutant). Fold changes were normalized to transcript levels of the wild type on P sufficiency (A) and ferric reductase activity of the wild type on Fe sufficiency (B). Data for P treatments were redrawn from Lei et al. (2011) with permission, and data for Fe were from García et al. (2010, 2014) and M.J. García, F.J. Romera, C. Lucena, E. Alcántara, and R. Pérez-Vicente (unpublished data).

Figure 3.

Ethylene (ET) could regulate different nutrient deficiency responses through two distinct signal transduction pathways. One pathway is CTR1-EIN2 dependent, and the other is CTR1-EIN2 independent (instead, using Arabidopsis His Phosphotransfer [AHP] proteins and Arabidopsis Response Regulators [ARRs]; Shakeel et al., 2013). This model is supported by data showing that ctr1 and ein2 mutants respond to both ACC and ET inhibitors for some physiological responses (García et al., 2007, 2010, 2014; Jung et al., 2009). It is possible that both pathways can act independently (A) or that both can interact and converge downstream through EIN3/EILs (B) depending on the responses (Table I). ─╢, Inhibition; →, promotion.

Figure 4.

Working model to explain the role of ethylene (ET) on the regulation of responses to different nutrient deficiencies in plants. Nutrient deficiencies can enhance ET production by up-regulating SAMS, ACS, and ACO genes (Shin and Schachtman, 2004; García et al., 2010; Hermans et al., 2010), although the steps leading to this up-regulation are not yet clear. A possibility is that, at first, nutrient deficiencies cause oxidative stress and consequently, ROS accumulation and possibly, NO accumulation (Shin et al., 2005; Tewari et al., 2006; Graziano and Lamattina, 2007; Ahlfors et al., 2009; Jung et al., 2009; García et al., 2011; Iqbal et al., 2013; Steffens, 2014). This ROS-NO accumulation would stimulate ET production, which in turn, could increase ROS-NO production (Ahlfors et al., 2009; Jung et al., 2009; García et al., 2011; Iqbal et al., 2013) in a positive feedback loop, leading to enhancement of the nutrient deficiency signal (García et al., 2011). When ET is perceived by the receptors, it could act through a CTR1-EIN2-dependent pathway for the regulation of some responses or a CTR1-EIN2-independent pathway for the regulation of other responses (Fig. 3). At the end of these transduction pathways, different ET-related transcription factors, such as RAP2.11, ERF070, EIL3, EIN3/EIL1, or others, would activate different nutrient responses (Maruyama-Nakashita et al., 2006; Kim et al., 2012; Ramaiah et al., 2014; Yang et al., 2014). Under nutrient sufficiency, several signals that can move through the phloem (mineral ions, peptides, GSH, etc.; Lappartient et al., 1999; García et al., 2013; Zhang et al., 2014) could negatively interact with ET to inactivate nutrient responses. However, under nutrient deficiency, other signals that can move through the phloem (microRNAs, auxin, sugars, etc.; Kasajima et al., 2007; Lejay et al., 2008; Hammond and White, 2011; Lei and Liu, 2011; Hu et al., 2015) could positively interact with ET to activate the responses. Additionally, ET can influence auxin accumulation and distribution and the expression of some microRNAs (see text for details). Yellow background indicates signals that activate responses, orange background indicates signals that repress responses. AHP, Arabidopsis His Phosphotransfer; ARR, Arabidopsis Response Regulators; ─╢, inhibition; →, promotion.