Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression

Abstract

The ATHB-2 gene encoding an homeodomain-leucine zipper protein is rapidly and strongly induced by changes in the ratio of red to far-red light which naturally occur during the daytime under the canopy and induce in many plants the shade avoidance response. Here, we show that elevated ATHB-2 levels inhibit cotyledon expansion by restricting cell elongation in the cotyledon-length and -width direction. We also show that elevated ATHB-2 levels enhance longitudinal cell expansion in the hypocotyl. Interestingly, we found that ATHB-2-induced, as well as shade-induced, elongation of the hypocotyl is dependent on the auxin transport system. In the root and hypocotyl, elevated ATHB-2 levels also inhibit specific cell proliferation such as secondary growth of the vascular system and lateral root formation. Consistent with the key role of auxin in these processes, we found that auxin is able to rescue the ATHB-2 lateral root phenotype. We also show that reduced levels of ATHB-2 result in reciprocal phenotypes. Moreover, we demonstrate that ATHB-2 functions as a negative regulator of gene expression in a transient assay. Remarkably, the expression in transgenic plants of a derivative of ATHB-2 with the same DNA binding specificity but opposite regulatory properties results in a shift in the orientation of hypocotyl cell expansion toward radial expansion, and in an increase in hypocotyl secondary cell proliferation. A model of ATHB-2 function in the regulation of shade-induced growth responses is proposed.

HD-ZIP Gene Family: Potential Roles in Improving Plant Growth and Regulating Stress-Responsive Mechanisms in Plants

“…The AtHB2/HAT4 is strongly induced under the dark condition in the etiolated seedlings [100]. To confirm their function, transgenic lines overexpressing AtHB2/HAT4 produced longer hypocotyls [101]. This indicated that AtHB2/HAT4 is responsible for controlling the growth of seedlings in fluctuating light conditions.…”

Triacylglycerol biosynthesis in shaded seeds of tung tree (Vernicia fordii) is regulated in part by Homeodomain Leucine Zipper 21

“…Some of the TFs we identified are closely related to members of the large HD‐ZIP class of transcriptional regulators; these were of particular interest to us here. Some members of this group have also been reported to be induced by shade and could promote the shade avoidance response (Carabelli et al., 2018; Sorin et al., 2009; Steindler et al., 1999). For example, ATHB1 , ATHB16 (both HD‐ZIP class I), ATHB2 , and ATHB4 (both HD‐ZIP class II) were reported to have a role in light responses (Aoyama et al., 1995; Carabelli et al., 1993, 1996; Sorin et al., 2009; Steindler et al., 1999; Wang et al., 2003).…”

“…Some members of this group have also been reported to be induced by shade and could promote the shade avoidance response (Carabelli et al., 2018; Sorin et al., 2009; Steindler et al., 1999). For example, ATHB1 , ATHB16 (both HD‐ZIP class I), ATHB2 , and ATHB4 (both HD‐ZIP class II) were reported to have a role in light responses (Aoyama et al., 1995; Carabelli et al., 1993, 1996; Sorin et al., 2009; Steindler et al., 1999; Wang et al., 2003). Two other class I HD‐ZIP TFs and one class II HD‐ZIP TF were in the core set of shade‐upregulated TFs identified in this study (Figure S9), namely VfHB7.1 , VfHB7.2 , and VfHAT22 .…”

“…These results reveal the identity and expression levels of the core TFs that are negatively correlated to oil accumulation and suggest that at least some of them may exert control over triacylglycerol metabolism during persistent dense shade conditions, even during the rapid oil accumulation period. Of the 32 genes encoding TFs, HD-ZIP genes from other plants had previously been reported to be induced by shade and to participate in the shade avoidance response (Carabelli et al, 2018;Sorin et al, 2009;Steindler et al, 1999). MYB59 (Mu et al, 2009), MYB3 (Mu et al, 2009), LUX ARRHYTHMO (Helfer et al, 2011), DIV2 (Fang et al, 2018), and GTL1 (Breuer et al, 2009(Breuer et al, , 2012 were all reported to negatively regulate different aspects of plant development.…”

MINI-EX: Integrative inference of single-cell gene regulatory networks in plants

“…Among these, 25 are TFs and 15 of these appeared as main regulators of the inferred regulons (Supplemental Table 2). Examples include genes known to be involved in root morphogenesis such as KNAT7 and HAT4 (Steindler et al, 1999;Zhong et al, 2008), but more interestingly, also genes with unknown functions such as AT2G03470 in xylem-31, WRKY3 in trichoblast-27, and bZIP6 in several stele-related clusters.…”