Arabidopsis LAZY1 is a peripheral membrane protein of which the carboxy-terminal fragment potentially interacts with microtubules

Sasaki, Shu; Yamamoto, Kotaro T.

doi:10.5511/plantbiotechnology.15.0106a

Cited by 12 publications

(10 citation statements)

References 22 publications

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“…Yet, the importance or specific role of each domain may vary between species. Heterologously expressed GFP-tagged full-length and truncated LAZY1 proteins, along with in vitro assays, indicated monocot and dicot LAZY1 proteins, as well as Arabidopsis AtLAZY2, 3 and 4, associate with the plasma membrane and, in some cases, microtubules and nuclei 4,5,20,28,29 . The LAZY1 TMD was needed for membrane localization of transiently expressed rice and maize LAZY1-GFP in onion 20,27 .…”

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Opposing influences of TAC1 and LAZY1 on Lateral Shoot Orientation in Arabidopsis

Hollender

Hill

Waite

et al. 2020

Sci Rep

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TAC1 and LAZY1 are members of a gene family that regulates lateral shoot orientation in plants. TAC1 promotes outward orientations in response to light, while LAZY1 promotes upward shoot orientations in response to gravity via altered auxin transport. We performed genetic, molecular, and biochemical assays to investigate possible interactions between these genes. In Arabidopsis they were expressed in similar tissues and double mutants revealed the wide-angled lazy1 branch phenotype, indicating it is epistatic to the tac1 shoot phenotype. Surprisingly, the lack of TAC1 did not influence gravitropic shoot curvature responses. Combined, these results suggest TAC1 might negatively regulate LAZY1 to promote outward shoot orientations. However, additional results revealed that TAC1-and LAZY1 influence on shoot orientation is more complex than a simple direct negative regulatory pathway. Transcriptomes of Arabidopsis tac1 and lazy1 mutants compared to wild type under normal and gravistimulated conditions revealed few overlapping differentially expressed genes. Overexpression of each gene did not result in major branch angle differences. Shoot tip hormone levels were similar between tac1, lazy1, and Col, apart from exceptionally elevated levels of salicylic acid in lazy1. The data presented here provide a foundation for future study of TAC1 and LAZY1 regulation of shoot architecture.Lateral organ orientation in both shoots and roots plays a key role in a plant's interaction with the environment and its ability to access resources such as light and water. The IGT gene family members TILLER ANGLE CONTROL 1 (TAC1) and the related set of LAZY genes are important regulators of lateral organ orientation 1,2 . These genes share four conserved amino acid regions or domains, and LAZY genes share an additional C-terminal domain 3,4 . TAC1 generally occurs as a single copy gene, but many species possess multiple LAZY genes, with six identified in Arabidopsis 2-8 . While the LAZY1 gene of Arabidopsis thaliana (Arabidopsis) contributes almost exclusively to shoot architecture, the remaining Arabidopsis LAZY genes primarily control root architecture 7,8 . However, GUS reporter activity and additive shoot phenotypes in plants with combinatorial lazy1, lazy2, and lazy4 mutations suggest LAZY2 and LAZY4 also have a role in regulating shoot orientation 7,8 . LAZY2, 3, and 4 are also known as DEEPER ROOTING (DRO3, 2, & 1) and NEGATIVE GRAVITROPIC RESPONSE OF ROOTS (NGR1, 3, & 2), respectively, as they were separately identified as regulators of lateral root orientation 6,9-12 . Further, an alternate LAZY gene nomenclature denotes LAZY3 as LZY2 and LAZY4 as LZ3Y 8 .Lateral branches, tillers, leaves, and flower buds of plants with loss-of-function tac1 mutations or reduced TAC1 expression exhibit upright orientations 3,13-19 . In contrast, lazy1 mutants have wider branch or tiller angles and lazy4/dro1 mutants display prostrate lateral root orientations 4-9,20-24 . Plants with multiple lazy/dro mutations exhibit even wider lateral shoot/root...

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confidence: 99%

Opposing influences of TAC1 and LAZY1 on Lateral Shoot Orientation in Arabidopsis

Hollender

Hill

Waite

et al. 2020

Sci Rep

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“…Arabidopsis LAZY1 (AtLAZY1) is also required for gravitropism in the inflorescence stem and seedling hypocotyl (Yoshihara et al, 2013). Branch angles are wider in atlazy1 as in oslazy1 (Yoshihara et al, 2013;Sasaki and Yamamoto, 2015) even though branch angle in monocots and dicots are determined by shoot structures that are not anatomically homologous. LAZY1 was shown to be required for auxin redistribution in response to gravitropic stimulation in rice (Oryza sativa; Godbole et al, 1999;Li et al, 2007;Yoshihara and Iino, 2007) and in maize (Zea mays; Dong et al, 2013).…”

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confidence: 99%

“…LAZY1 was shown to be required for auxin redistribution in response to gravitropic stimulation in rice (Oryza sativa; Godbole et al, 1999;Li et al, 2007;Yoshihara and Iino, 2007) and in maize (Zea mays; Dong et al, 2013). OsLAZY1, ZmLAZY1, and AtLAZY1 localize to the nucleus and at the cell periphery, probably including the plasma membrane (Dong et al, 2013;Yoshihara et al, 2013;Howard et al, 2014;Sasaki and Yamamoto, 2015). The rice Deeper Rooting1 (OsDRO1) is also a LAZY family gene (Yoshihara et al, 2013).…”

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

2017

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A rice (Oryza sativa) mutant led to the discovery of a plant-specific LAZY1 protein that controls the orientation of shoots. Arabidopsis (Arabidopsis thaliana) possesses six LAZY genes having spatially distinct expression patterns. Branch angle phenotypes previously associated with single LAZY genes were here studied in roots and shoots of single and higher-order atlazy mutants. The results identify the major contributors to root and shoot branch angles and gravitropic behavior of seedling hypocotyls and primary roots. AtLAZY1 is the principal determinant of inflorescence branch angle. The weeping inflorescence phenotype of atlazy1,2,4 mutants may be due at least in part to a reversal in the gravitropism mechanism. AtLAZY2 and AtLAZY4 determined lateral root branch angle. Lateral roots of the atlazy2,4 double mutant emerged slightly upward, approximately 10°g reater than perpendicular to the primary root axis, and they were agravitropic. Etiolated hypocotyls of the quadruple atlazy1,2,3,4 mutant were essentially agravitropic, but their phototropic response was robust. In light-grown seedlings, the root of the atlazy2,3,4 mutant was also agravitropic but when adapted to dim red light it displayed a reversed gravitropic response. A reversed auxin gradient across the root visualized by a fluorescent signaling reporter explained the reversed, upward bending response. We propose that AtLAZY proteins control plant architecture by coupling gravity sensing to the formation of auxin gradients that override a LAZY-independent mechanism that creates an opposing gravity-induced auxin gradient.

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“…In contrast, Li et al (2019) demonstrated that rice LAZY1 lacking a nuclear localization signal was unable to rescue an oslazy1 mutant phenotype. Sasaki and Yamamoto (2015) showed that AtLAZY1 is a peripheral PM protein but found that the C-terminal domain by itself associates with microtubules (Sasaki and Yamamoto 2015). Our observation that AtDRO1 protein was detectable in nuclei in root tips under native conditions suggests that localization to the PM is likely mediated by specific signals, cell-type specific interacting proteins, and/or conditions.…”

Section: Discussionmentioning

confidence: 99%

“…This motif has been shown in wheat DRO1 to facilitate interaction with the TOPLESS protein at the plasma membrane and nucleus (Ashraf et al 2019). Other conserved domains have been characterized within the similar LAZY1 protein to be important for nuclear localization, plasma membrane localization, and association with microtubules using transient assays in protoplasts, and Arabidopsis and N. benthamiana leaves (Yoshihara et al 2013;Sasaki and Yamamoto 2015;Yoshihara and Spalding 2019). AtDRO1 protein driven by an estradiol-inducible promoter, was found to localize to the membranes of root epidermal and lateral root cap cells (Ge and Chen 2019).…”

Section: Introductionmentioning

confidence: 99%

AtDRO1 is nuclear localized in root tips under native conditions and impacts auxin localization

2020

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DEEPER ROOTING 1 (DRO1) contributes to the downward gravitropic growth trajectory of roots upstream of lateral auxin transport in monocots and dicots. Loss of DRO1 function leads to horizontally oriented lateral roots and altered gravitropic set point angle, while loss of all three DRO family members results in upward, vertical root growth. Here, we attempt to dissect the roles of AtDRO1 by analyzing expression, protein localization, auxin gradient formation, and auxin responsiveness in the atdro1 mutant. Current evidence suggests AtDRO1 is predominantly a membrane-localized protein. Here we show that VENUS-tagged AtDRO1 driven by the native AtDRO1 promoter complemented an atdro1 Arabidopsis mutant and the protein was localized in root tips and detectable in nuclei. atdro1 primary and lateral roots showed impairment in establishing an auxin gradient upon gravistimulation as visualized with DII-VENUS, a sensor for auxin signaling and proxy for relative auxin distribution. Additionally, PIN3 domain localization was not significantly altered upon gravistimulation in atdro1 primary and lateral roots. RNA-sequencing revealed differential expression of known root development-related genes in atdro1 mutants. atdro1 lateral roots were able to respond to exogenous auxin and AtDRO1 gene expression levels in root tips were unaffected by the addition of auxin. Collectively, the data suggest that nuclear localization may be important for AtDRO1 function and suggests a more nuanced role for DRO1 in regulating auxin-mediated changes in lateral branch angle. Key message DEEPER ROOTING 1 (DRO1) when expressed from its native promoter is predominately localized in Arabidopsis root tips, detectable in nuclei, and impacts auxin gradient formation.

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Arabidopsis LAZY1 is a peripheral membrane protein of which the carboxy-terminal fragment potentially interacts with microtubules

Cited by 12 publications

References 22 publications

Opposing influences of TAC1 and LAZY1 on Lateral Shoot Orientation in Arabidopsis

Opposing influences of TAC1 and LAZY1 on Lateral Shoot Orientation in Arabidopsis

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

AtDRO1 is nuclear localized in root tips under native conditions and impacts auxin localization

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