SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in<i>Arabidopsis</i>

Spartz, Angela; Ren, Hong Yu; Park, Mee Yeon; Grandt, Kristin N.; Lee, Sang Ho; Murphy, Angus S.; Sussman, Michael R.; Overvoorde, Paul J.; Gray, William M.

doi:10.1105/tpc.114.126037

Cited by 415 publications

(539 citation statements)

References 68 publications

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“…The more sustained shade induction of numerous auxin response genes in hypocotyls ( Figure 4A) is consistent with the notion that an organ-specific auxin response contributes to selective hypocotyl elongation (Bou-Torrent et al, 2014;Hersch et al, 2014;de Wit et al, 2015;Sun et al, 2016). Hypocotylspecific induction of many (but not all) SAUR genes is also consistent with this idea ( Figure 5) (Spartz et al, 2014;Ren and Gray, 2015). Our data also support a role for BL in defining organ-specific growth.…”

Section: Discussionsupporting

confidence: 78%

“…Interestingly, the hypocotyl of these mutants was undistinguishable from the wild type in high R/FR, while in low R/FR, it was slightly but significantly shorter (Supplemental Figure 4I). This finding is consistent with the positive role of SAURs in elongation growth (Spartz et al, 2012(Spartz et al, , 2014. Finally, to test whether both the YUC-dependent and independent responses required the PIFs, we analyzed the expression of IAA1 and SAUR22 in pif4 pif5 pif7 hypocotyls and cotyledons and found that low R/FR induction of these genes was strongly attenuated in the pif triple mutant (Supplemental Figures 4J and 4K).…”

Section: Shade-regulated Expression Of a Subset Of Auxinresponsive Gesupporting

confidence: 57%

“…We used the following Arabidopsis thaliana genotypes (cv Columbia-0): pin3 pin4 pin7, d6pk01, D6PK-OX (Willige et al, 2013), sav3-2 (Tao et al, 2008), pif7-1 (Li et al, 2012), DII-VENUS (Brunoud et al, 2012), pif4 pif5 pif7 (de Wit et al, 2015), amiD2/5/7/8/9 (Spartz et al, 2014), amiSAUR19/23/24 (Spartz et al, 2012), and iYUC3 (FRO6:XVE:YUC3; Chen et al, 2014). To generate the yuc2 yuc5 yuc8 yuc9 quadruple mutant, T-DNA and transposon insertion lines were obtained from the ABRC, the Cold Spring Harbor Laboratory, or GABI-Kat.…”

Section: Plant Growth and Light Conditionsmentioning

confidence: 99%

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Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

et al. 2016

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ORCID IDs: 0000-0001-5075-575X (M.V.K.); 0000-0003-1339-5120 (E.S.-S.); 0000-0002-4145-7205 (F.S.); 0000-0001-9237-1797 (P.M.-M.); 0000-0002-9623-2599 (J.M.); 0000-0002-3413-6841 (I.X.); 0000-0003-4719-5901 (C.F.)In response to neighbor proximity, plants increase the growth of specific organs (e.g., hypocotyls) to enhance access to sunlight. Shade enhances the activity of Phytochrome Interacting Factors (PIFs) by releasing these bHLH transcription factors from phytochrome B-mediated inhibition. PIFs promote elongation by inducing auxin production in cotyledons. In order to elucidate spatiotemporal aspects of the neighbor proximity response, we separately analyzed gene expression patterns in the major light-sensing organ (cotyledons) and in rapidly elongating hypocotyls of Arabidopsis thaliana. PIFs initiate transcriptional reprogramming in both organs within 15 min, comprising regulated expression of several early auxin response genes. This suggests that hypocotyl growth is elicited by both local and distal auxin signals. We show that cotyledon-derived auxin is both necessary and sufficient to initiate hypocotyl growth, but we also provide evidence for the functional importance of the local PIFinduced response. With time, the transcriptional response diverges increasingly between organs. We identify genes whose differential expression may underlie organ-specific elongation. Finally, we uncover a growth promotion gene expression signature shared between different developmentally regulated growth processes and responses to the environment in different organs.

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Section: Discussionsupporting

confidence: 78%

Section: Shade-regulated Expression Of a Subset Of Auxinresponsive Gesupporting

confidence: 57%

Section: Plant Growth and Light Conditionsmentioning

confidence: 99%

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Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

et al. 2016

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“…Of 175 K4-SDRGs that displayed a loss of H3K4me3 marks and decreased gene expression, 13 encoded YUCCA-and SAUR-like genes involved in auxin biosynthesis Stepanova et al, 2011;Won et al, 2011) and response, respectively (Spartz et al, 2012(Spartz et al, , 2014. Auxin synthesis sets in motion major changes in gene expression and physiology (Guilfoyle and Hagen, 2007), and the down-regulation of auxin synthesis and signaling can be considered a primary event in the progression of senescence.…”

Section: Discussionmentioning

confidence: 99%

A Genome-Wide Chronological Study of Gene Expression and Two Histone Modifications, H3K4me3 and H3K9ac, during Developmental Leaf Senescence

et al. 2015

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The genome-wide abundance of two histone modifications, H3K4me3 and H3K9ac (both associated with actively expressed genes), was monitored in Arabidopsis (Arabidopsis thaliana) leaves at different time points during developmental senescence along with expression in the form of RNA sequencing data. H3K9ac and H3K4me3 marks were highly convergent at all stages of leaf aging, but H3K4me3 marks covered nearly 2 times the gene area as H3K9ac marks. Genes with the greatest fold change in expression displayed the largest positively correlated percentage change in coverage for both marks. Most senescence up-regulated genes were premarked by H3K4me3 and H3K9ac but at levels below the whole-genome average, and for these genes, gene expression increased without a significant increase in either histone mark. However, for a subset of genes showing increased or decreased expression, the respective gain or loss of H3K4me3 marks was found to closely match the temporal changes in mRNA abundance; 22% of genes that increased expression during senescence showed accompanying changes in H3K4me3 modification, and they include numerous regulatory genes, which may act as primary response genes.

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“…H + -ATPases to promote cell expansion (29). Although the understanding of the functions and molecular mechanisms of SAURs remains rudimentary, current data suggest that SAURs may play key roles in integrating multiple signals into distinct growth and developmental responses (22).…”

Section: Significancementioning

confidence: 99%

Arabidopsis SAURs are critical for differential light regulation of the development of various organs

Sun

Wang

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

137

186

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During deetiolation of Arabidopsis seedlings, light promotes the expansion of cotyledons but inhibits the elongation of hypocotyls. The mechanism of this differential regulation of cell enlargement is unclear. Our organ-specific transcriptomic analysis identified 32 Small Auxin Up RNA (SAUR) genes whose transcripts were light-induced in cotyledons and/or repressed in hypocotyls. We therefore named these SAURs as lirSAURs. Both overexpression and mutation analyses demonstrated that lirSAURs could promote cotyledon expansion and opening and enhance hypocotyl elongation, possibly by inhibiting phosphatase activity of D-clade type 2C protein phosphatases (PP2C-Ds). Light reduced auxin levels to down-regulate the expression of lirSAURs in hypocotyls. Further, phytochrome-interacting factors (PIFs) were shown to directly bind the genes encoding these SAURs and differentially regulate their expression in cotyledons and hypocotyls. Together, our study demonstrates that light mediates auxin levels and PIF stability to differentially regulate the expression of lirSAURs in cotyledons and hypocotyls, and these lirSAURs further mediate the differential growth of these two organs.light signal | seedling development | SAURs | auxin | PIFs

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SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion inArabidopsis

Cited by 415 publications

References 68 publications

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

A Genome-Wide Chronological Study of Gene Expression and Two Histone Modifications, H3K4me3 and H3K9ac, during Developmental Leaf Senescence

Arabidopsis SAURs are critical for differential light regulation of the development of various organs

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