The Arabidopsis LAZY1 Family Plays a Key Role in Gravity Signaling within Statocytes and in Branch Angle Control of Roots and Shoots

Abstract

ORCID IDs: 0000-0003-4414-0649 (H.T.); 0000-0002-9657-8231 (M. Tasaka); 0000-0002-6176-5758 (M.T.M.)During gravitropism, the directional signal of gravity is perceived by gravity-sensing cells called statocytes, leading to asymmetric distribution of auxin in the responding organs. To identify the genes involved in gravity signaling in statocytes, we performed transcriptome analyses of statocyte-deficient Arabidopsis thaliana mutants and found two candidates from the LAZY1 family, AtLAZY1/LAZY1-LIKE1 (LZY1) and AtDRO3/AtNGR1/LZY2. We showed that LZY1, LZY2, and a paralog AtDRO1/AtNGR2/LZY3 are redundantly involved in gravitropism of the inflorescence stem, hypocotyl, and root. Mutations of LZY genes affected early processes in gravity signal transduction without affecting amyloplast sedimentation. Statocyte-specific expression of LZY genes rescued the mutant phenotype, suggesting that LZY genes mediate gravity signaling in statocytes downstream of amyloplast displacement, leading to the generation of asymmetric auxin distribution in gravity-responding organs. We also found that lzy mutations reversed the growth angle of lateral branches and roots. Moreover, expression of the conserved C-terminal region of LZY proteins also reversed the growth direction of primary roots in the lzy mutant background. In lateral root tips of lzy multiple mutants, asymmetric distribution of PIN3 and auxin response were reversed, suggesting that LZY genes regulate the direction of polar auxin transport in response to gravity through the control of asymmetric PIN3 expression in the root cap columella.

LAZY Genes Mediate the Effects of Gravity on Auxin Gradients and Plant Architecture

“…It remains to be determined if auxin affects the expression of other LAZY family genes. Taniguchi et al (2017) reported function of LAZY genes while our report was being revised. They reported the control of inflorescence stem gravitropism by AtLAZY1, AtLAZY2, and AtLAZY4, supporting the results in Figure 6.…”

“…4). Taniguchi et al (2017) further showed that AtLAZY genes control the PIN3 expression pattern in the lateral root tip. This can explain the lack of auxin redistribution in lazy mutants (Godbole et al, 1999;Li et al, 2007;Yoshihara and Iino, 2007;Dong et al, 2013) and emergence of reversed auxin redistribution in atlazy2,3,4 (Fig.…”

Antagonistic and auxin-dependent phosphoregulation of columella PIN proteins controls lateral root gravitropic setpoint angle in Arabidopsis

“…We also do not exclude other mechanisms contributing to GSA control in the lateral root. In particular, it will be interesting to establish the level at which LAZY proteins, recently shown to play a role in primary and lateral root gravitropism (Ge & Chen, 2016;Guseman et al, 2017;Taniguchi et al, 2017;, input into the control of PIN polarity in lateral root statocytes and how their activity integrates with the phosphoregulation of PIN3 identified here. Perhaps the most conspicuous open question at hand is a very old one, that of how statolith sedimentation is turned into asymmetry in PIN localisation and activity within statocytes.…”

Arabidopsis ANAC092 regulates auxin‐mediated root development by binding to the ARF8 and PIN4 promoters

“…Earlier investigations concluded that starch grains acting as statocytes in the root cap affect primary root development (Taniguchi et al ). We also stained the starch grains in the root cap, using an iodine‐iodide pokalium (I 2 ‐KI) solution, and observed that the layers and sizes of starch grains were unchanged in the ANAC092 ‐overexpressing plants (Figure S2A).…”