Gravity-Sensing Tissues for Gravitropism Are Required for “Anti-Gravitropic” Phenotypes of lzy Multiple Mutants in Arabidopsis

Abstract

Plant posture is controlled by various environmental cues, such as light, temperature, and gravity. The overall architecture is determined by the growth angles of lateral organs, such as roots and branches. The branch growth angle affected by gravity is known as the gravitropic setpoint angle (GSA), and it has been proposed that the GSA is determined by balancing two opposing growth components: gravitropism and anti-gravitropic offset (AGO). The molecular mechanisms underlying gravitropism have been studied extensively, but little is known about the nature of the AGO. Recent studies reported the importance of LAZY1-LIKE (LZY) family genes in the signaling process for gravitropism, such that loss-of-function mutants of LZY family genes resulted in reversed gravitropism, which we term it here as the “anti-gravitropic” phenotype. We assume that this peculiar phenotype manifests as the AGO due to the loss of gravitropism, we characterized the “anti-gravitropic” phenotype of Arabidopsis lzy multiple mutant genetically and physiologically. Our genetic interaction analyses strongly suggested that gravity-sensing cells are required for the “anti-gravitropic” phenotype in roots and lateral branches. We also show that starch-filled amyloplasts play a significant role in the “anti-gravitropic” phenotype, especially in the root of the lzy multiple mutant.

The shaping of plant axes and crowns through tropisms and elasticity: an example of morphogenetic plasticity beyond the shoot apical meristem

“…5a‐2), transmitting the control of the tropic movement to the active bending motors (the expanding cells), according to the classical Cholodny–Went model (see Moulia et al ., 2019; Nakamura et al ., 2019 for further recent reviews). The TAC1 protein is also present in the statocytes (Kawamoto et al ., 2020) but its cellular role is unknown. Because the statocytes are organised into a sheath of cells that spans all along the shoot (in the endodermis in young stems (Morita, 2010), in the secondary phloem in woody stems; Gerttula et al ., 2015), this provides the stem with the ability to sense the inclination angle vs the direction of the gravity A ( s ) all along the stem, and to react at each place through gravitropic bending.…”

“…(2013) proposed another model: the antigravitropic offset model (AGO), which is receiving increasing experimental support by Kawamoto et al . (2020). They showed that when lateral branches of Arabidopsis are continuously clinorotated (to prevent the gravitropic sensing), they display extensive outward curvature (Fig.…”

Gravity Signaling in Flowering Plant Roots

“…This offset mechanism is best observed in lzy2 lzy3 lzy4 triple mutant roots, which show opposite GSA relative to wild type [ 82 , 90 , 115 ], and in lzy mutant plants that express a mutated form of AtLAZY1 carrying two conserved amino acid substitutions in region II of the protein [ 90 ]. Its function requires the presence of functional gravity-sensing statocytes with starch-filled sedimenting amyloplasts [ 116 ], and involves cytokinin signaling, which interferes with growth at the upper flank of the lateral roots [ 117 ].…”

“…TAC1 was proposed to function as an integrator between light perception and LAZY1-mediated gravity response to optimize shoot position for light capture. Unfortunately, a role for TAC1 in regulating the antigravitropic offset mechanism in lateral roots is unlikely because its expression is very low in these organs [ 116 ]. Recent identification of three genetic suppressors of lzy2 lzy3 lzy4 and their characterization may yield interesting new insights into the machinery that governs the antigravitropic offset mechanism in lateral roots [ 116 ].…”

IGT/LAZY family genes are differentially influenced by light signals and collectively required for light-induced changes to branch angle

“…Recent studies have demonstrated that LAZY and DRO genes influence organ orientation downstream of amyloplast sedimentation and upstream of auxin localization (Taniguchi et al, 2017;Yoshihara and Spalding, 2017;Nakamura et al, 2019). In the roots, the "anti-gravitropic" phenotype of a lazy dro quadruple mutant requires functional statoliths, and in the shoot requires functional endodermal cells (Kawamoto et al, 2020). Mechanistic studies on DRO1 have shown that the protein is localized to the nucleus under native conditions in roots tips.…”