Deciphering Auxin-Ethylene Crosstalk at a Systems Level

Abstract

The auxin and ethylene pathways cooperatively regulate a variety of developmental processes in plants. Growth responses to ethylene are largely dependent on auxin, the key regulator of plant morphogenesis. Auxin, in turn, is capable of inducing ethylene biosynthesis and signaling, making the interaction of these hormones reciprocal. Recent studies discovered a number of molecular events underlying auxin-ethylene crosstalk. In this review, we summarize the results of fine-scale and large-scale experiments on the interactions between the auxin and ethylene pathways in Arabidopsis. We integrate knowledge on molecular crosstalk events, their tissue specificity, and associated phenotypic responses to decipher the crosstalk mechanisms at a systems level. We also discuss the prospects of applying systems biology approaches to study the mechanisms of crosstalk between plant hormones.

Keywords: apical hook; lateral root development; mathematical modeling; phytohormone; root elongation; root hair formation; transcriptional regulation.

Figure 1

Transcriptional regulation of auxin-related genes by ethylene precursor ACC in Arabidopsis root. The datasets from Harkey et al. [20] were analyzed. Only genes with significant expression changes (Benjamini-Hochberg FDR < 0.05) are shown in the heatmap. We omitted the data for 0.5, 1 and 2 h time points, as there were only few differentially-expressed genes under this criterion. “Other” are the rest of genes from TAA1/TAR, YUC, PIN, Aux/LAX, PILS, TIR/AFB, ARF, Aux/IAA families and auxin-related genes from ABCB, GH3 families.

Figure 2

Transcriptional regulation of ethylene-related genes by IAA in the Arabidopsis root. The datasets from Lewis et al. [19] were analyzed. Only the genes with significant expression changes (Benjamini-Hochberg FDR < 0.05) are shown in the heatmap. “Other” are the rest of genes from ACS, ACO families and the genes involved in ethylene signaling and overviewed in chapter 1.

Figure 3

Schematic representation of Arabidopsis seedling structure. On the left panel the root top (i.), root hair forming region (ii.), the zone of mature root (iii.) and apical hook (iv.) are highlighted. On the right panel the root tip structure is detailed. MZ—meristematic zone; TZ—transition zone; EZ—elongation zone.

Figure 4

The models of ethylene-induced auxin accumulation in the root tip (a) and ethylene induced auxin depletion in the root mature zone (b). (a) To regulate root growth, ethylene principally targets LRC and epidermis in the meristematic and early elongation zones in the root tip (zone i. in Figure 3). Upon perception in these tissues, ethylene affects local auxin biosynthesis through TAA1 accumulation in epidermal cells and ASA1, ASB1, and TAR2 induction (tissue specificity is unknown), and enhances shootward auxin transport in the LRC and epidermis by increasing AUX1 and PIN2 abundance. As a result, auxin accumulation in the outer layers of the root tip restricts root elongation. This model is based on the findings reported previously [21,22,24,25,27,30,44]. (b) In parallel with (a) ethylene induces PIN3 and PIN7 accumulation in the central cylinder of the whole root and blocks local AUX1 accumulation in the pericycle cells at the sites of lateral root initiation in the mature root (zone iii. in Figure 3). As a result, both enhanced rootward auxin transport through the central cylinder and reduced local auxin uptake in the pericycle prevent local auxin maxima formation required for lateral root primordia initiation. This model is based on the findings reported in Lewis et al. [26]. Dashed lines mark regulatory events with unknown mechanisms. LRC—lateral root cap. Question mark denotes the regulations with unknown tissue specificity.

Figure 5

The model of ethylene influence on auxin distribution asymmetry during apical hook formation. In the hook (zone iv. in Figure 3), ethylene activates expression of HLS1, which negatively regulates ARF2 levels to mediate asymmetric auxin distribution. Ethylene treatment downregulates PIN4, upregulates PIN3 and PIN7 expression in the epidermal cells of the hook. Simultaneously TAR2 and AUX1 expression is induced on the concave side of the apical hook. As a result, ethylene fine-tunes auxin maximum formation on the concave side of the hook. Dashed lines mark the regulatory events with unknown mechanisms, question marks highlight putative regulations. The triangles conditionally depict spatial molecular gradients. This model is based on findings reported previously [12,53,54].

Figure 6

The model of auxin-ethylene crosstalk during root hair development. Auxin redistribution contributes to the ethylene effects on planar polarity of root hair-forming cell and root hair growth (zone ii. in Figure 3). However, ethylene acts independently of auxin redistribution as well. EIN3 directly interacts with RHD6 to regulate root hair initiation and elongation. Dashed lines mark the regulatory events with unknown mechanisms. Red line marks protein-protein interaction. This model is based on findings reported previously [59,63,64,65].