Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis

Mudgil, Yashwanti; Karve, Abhijit; Teixeira, Paulo José Pereira Lima; Jiang, Kun; Tunc‐Ozdemir, Meral; Jones, Alan M.

doi:10.3389/fpls.2016.01255

Cited by 32 publications

(20 citation statements)

References 88 publications

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“…MRD1, is minimally characterized as of now, with the exception that it is downregulated in mto1-1 mutants that over-accumulate methionine. However, this gene in the root system architecture mutant agb1-2 was found to be co-expressed with At3g01345, the most highly induced gene in shoot tips from upright tac1 plants 40 . Connections between MRD1, At3g01345, TAC1, and LAZY1 warrant further investigation, as the functions of both are not understood.…”

Section: Discussionmentioning

confidence: 93%

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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Section: Discussionmentioning

confidence: 93%

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

Hollender

Hill

Waite

et al. 2020

Sci Rep

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“…Approximately half of the fixed CO 2 is immediately converted to starch while the rest is mobilized (Mengin et al., ; Sharkey, Berry, & Raschke, ; Sulpice et al., ). Given the rapid speed that fixed carbon reaches distal cells (Mudgil et al., ), we hypothesized that the extracellular sugars that are detected by AtRGS1 are derived by CO 2 fixation. As such, detection of G signaling activation in response to illumination is expected.…”

Section: Resultsmentioning

confidence: 99%

“…Fixed carbon in the leaf is rapidly distributed as sugars to sink tissue in plants with rates of movement ~1 cm per minute (Mudgil et al., ); thus, sugars are candidates for the long‐distance activator. To determine whether a sugar is the photosynthesis‐dependent product that activates G signaling, cotyledons were excised and replaced with a ¼x MS agar cube containing 6% D‐glucose.…”

Section: Resultsmentioning

confidence: 99%

Long‐distance communication in Arabidopsis involving a self‐activating G protein

et al. 2018

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In plant cells, heterotrimeric G protein signaling mediates development, biotic/abiotic stress responsiveness, hormone signaling, and extracellular sugar sensing. The amount of sugar in plant cells fluctuates from nanomolar to high millimolar concentrations over time depending on changes in the light environment. Arabidopsis thaliana Regulator of G Signaling protein 1 (AtRGS1) modulates G protein activation and detects the concentration and the exposure time of sugars. This is called dose–duration reciprocity in sugar sensing and occurs through AtRGS1 internalization which is directly proportional to G protein activation. One source of sugars is from CO2 fixation by photosynthesis. Through a simple set of experiments, we show that sugars made in cotyledons that are undergoing photomorphogenesis activate G signaling in cells distal to the nascent photosynthesis center. This occurs with sufficient speed to enable distal cells to monitor changes in photosynthetic activity in the leaves.

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“…Heterotrimeric G protein plays multiple roles in plant growth and development. Loss-of-function mutants of heterotrimeric G protein displayed altered shoot meristem growth (Bommert et al, 2013 ), zygote division (Yu et al, 2016 ), seedling development (Chen et al, 2006 ; Booker et al, 2010 ; Jaffe et al, 2012 ), root architecture (Mudgil et al, 2016 ) and resistance to pathogens (Llorente et al, 2005 ; Trusov et al, 2006 ; Liu et al, 2013 ). In eATP-induced responses, heterotrimeric G protein participated in stomatal movement (Hao et al, 2012 ) and obstacle avoidance of roots (Weerasinghe et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

Heterotrimeric G Protein-Regulated Ca2+ Influx and PIN2 Asymmetric Distribution Are Involved in Arabidopsis thaliana Roots' Avoidance Response to Extracellular ATP

et al. 2017

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Extracellular ATP (eATP) has been reported to be involved in plant growth as a primary messenger in the apoplast. Here, roots of Arabidopsis thaliana seedlings growing in jointed medium bent upon contact with ATP-containing medium to keep away from eATP, showing a marked avoidance response. Roots responded similarly to ADP and bz-ATP but did not respond to AMP and GTP. The eATP avoidance response was reduced in loss-of-function mutants of heterotrimeric G protein α subunit (Gα) (gpa1-1 and gpa1-2) and enhanced in Gα-over-expression (OE) lines (wGα and cGα). Ethylenebis(oxyethylenenitrilo) tetraacetic acid (EGTA) and Gd3+ remarkably suppressed eATP-induced root bending. ATP-stimulated Ca2+ influx was impaired in Gα null mutants and increased in its OE lines. DR5-GFP and PIN2 were asymmetrically distributed in ATP-stimulated root tips, this effect was strongly suppressed by EGTA and diminished in Gα null mutants. In addition, some eATP-induced genes' expression was also impaired in Gα null mutants. Based on these results, we propose that heterotrimeric Gα-regulated Ca2+ influx and PIN2 distribution may be key signaling events in eATP sensing and avoidance response in Arabidopsis thaliana roots.

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Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis

Cited by 32 publications

References 88 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

Long‐distance communication in Arabidopsis involving a self‐activating G protein

Heterotrimeric G Protein-Regulated Ca2+ Influx and PIN2 Asymmetric Distribution Are Involved in Arabidopsis thaliana Roots' Avoidance Response to Extracellular ATP

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