Cytokinin response factors regulate PIN-FORMED auxin transporters

Šimášková, Mária; O’Brien, José Antonio; Khan, Mamoona; Noorden, Giel Van; Ötvös, Krisztina; Vieten, Anne; Clercq, Inge De; Haperen, Johanna Maria Adriana Van; Cuesta, Candela; Hoyerová, Klára; Vanneste, Steffen; Marhavý, Peter; Wabnik, Krzysztof; Breusegem, Frank Van; Nowack, Moritz K.; Murphy, Angus S.; Friml, Jiřı́; Weijers, Dolf; Beeckman, Tom; Benková, Eva

doi:10.1038/ncomms9717

Cited by 121 publications

(82 citation statements)

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“…2009; Bishopp et al, 2011;Šimášková et al, 2015). Together our data suggest that YUC1 and PIN7 expression overlap with peak cytokinin signaling in the subapical medial tissue of the gynoecial primordium, and that cytokinin can promote medial auxin biosynthesis in, and PIN7-mediated auxin efflux from, this domain.…”

Section: Cytokinin Promotes Auxin Biosynthesis Gene Activity and Regumentioning

confidence: 59%

“…In roots, cytokinin signaling can regulate the expression of several YUC auxin biosynthesis genes (Jones et al, 2010;Di et al, 2016), and PIN1, PIN3, and PIN7 auxin efflux carriers (Dello Ioio et al, 2008;Ruzicka et al, 2009;Bishopp et al, 2011;Šimášková et al, 2015). We and others have previously shown that PIN1, PIN3, and PIN7 translational reporters are expressed in tissue-specific patterns in early stage gynoecial primordia (Larsson et al, 2014;Moubayidin and Ostergaard, 2014).…”

Section: Cytokinin Promotes Auxin Biosynthesis Gene Activity and Regumentioning

confidence: 96%

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Cytokinin-Auxin Crosstalk in the Gynoecial Primordium Ensures Correct Domain Patterning

et al. 2017

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The Arabidopsis (Arabidopsis thaliana) gynoecium consists of two congenitally fused carpels made up of two lateral valve domains and two medial domains, which retain meristematic properties and later fuse to produce the female reproductive structures vital for fertilization. Polar auxin transport (PAT) is important for setting up distinct apical auxin signaling domains in the early floral meristem remnants allowing for lateral domain identity and outgrowth. Crosstalk between auxin and cytokinin plays an important role in the development of other meristematic tissues, but hormone interaction studies to date have focused on more accessible later-stage gynoecia and the spatiotemporal interactions pivotal for patterning of early gynoecium primordia remain unknown. Focusing on the earliest stages, we propose a cytokinin-auxin feedback model during early gynoecium patterning and hormone homeostasis. Our results suggest that cytokinin positively regulates auxin signaling in the incipient gynoecial primordium and strengthen the concept that cytokinin regulates auxin homeostasis during gynoecium development. Specifically, medial cytokinin promotes auxin biosynthesis components [YUCCA1/4 (YUC1/4)] in, and PINFORMED7 (PIN7)-mediated auxin efflux from, the medial domain. The resulting laterally focused auxin signaling triggers ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN6 (AHP6), which then represses cytokinin signaling in a PAT-dependent feedback. Cytokinin also down-regulates PIN3, promoting auxin accumulation in the apex. The yuc1, yuc4, and ahp6 mutants are hypersensitive to exogenous cytokinin and 1-napthylphthalamic acid (NPA), highlighting their role in mediolateral gynoecium patterning. In summary, these mechanisms self-regulate cytokinin and auxin signaling domains, ensuring correct domain specification and gynoecium development.

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Section: Cytokinin Promotes Auxin Biosynthesis Gene Activity and Regumentioning

confidence: 59%

Section: Cytokinin Promotes Auxin Biosynthesis Gene Activity and Regumentioning

confidence: 96%

Cytokinin-Auxin Crosstalk in the Gynoecial Primordium Ensures Correct Domain Patterning

et al. 2017

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“…LR numbers of both crf2,5,6 and crf3,5,6 triple mutants were reduced compared with the wild type (Raines et al, 2016). Loss-offunction mutations in CRF2 or CRF3 or both CRF3 and CRF6 or CRF2, CRF3, and CRF6 caused reductions in root length, root meristem size, and LRP density, whereas overexpression of CRF2 or CRF3 or CRF6 enhanced LRP density ( Simá sková et al, 2015). In addition, multiple mutations in CRFs result in larger rosettes, delayed leaf senescence, and shorter hypocotyls in etiolated seedlings (Raines et al, 2016).…”

Section: Discussionmentioning

confidence: 92%

“…This study demonstrated that CRF2 and CRF3 play an important role during LR development in Arabidopsis and also integrate the cold signal into LR development for an adaptation response to cold stress via signaling pathways as depicted in the model (Figure 8). A recent study showed that CRF2 and CRF6 transcriptionally control genes encoding PIN-FORMED (PIN) auxin transporters such as PIN1 and PIN7, providing a crosstalk component that fine-tunes auxin transport capacity downstream of cytokinin signaling to control plant growth and development ( Simá sková et al, 2015). Therefore, CRF2 and CRF3 gate endogenous hormone signals, such as cytokinin and auxin, as well as the environmental cold signal, providing adaptation versatility to the plants under cold stress.…”

Section: Discussionmentioning

confidence: 99%

CYTOKININ RESPONSE FACTOR2 (CRF2) and CRF3 Regulate Lateral Root Development in Response to Cold Stress in Arabidopsis

et al. 2016

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ORCID IDs: 0000-0001-7997-1544 (C.C.); 0000-0003-1735-5564 (J.K.)Lateral roots (LRs) are a major determinant of the root system architecture in plants, and developmental plasticity of LR formation is critical for the survival of plants in changing environmental conditions. In Arabidopsis thaliana, genetic pathways have been identified that regulate LR branching in response to numerous environmental cues, including some nutrients, salt, and gravity. However, it is not known how genetic components are involved in the LR adaptation response to cold. Here, we demonstrate that CYTOKININ RESPONSE FACTOR2 (CRF2) and CRF3, encoding APETALA2 transcription factors, play an important role in regulating Arabidopsis LR initiation under cold stress. Analysis of LR developmental kinetics demonstrated that both CRF2 and CRF3 regulate LR initiation. crf2 and crf3 single mutants exhibited decreased LR initiation under cold stress compared with the wild type, and the crf2 crf3 double mutants showed additively decreased LR densities compared with the single mutants. Conversely, CRF2 or CRF3 overexpression caused increased LR densities. CRF2 was induced by cold via a subset of the cytokinin two-component signaling (TCS) pathway, whereas CRF3 was upregulated by cold via TCSindependent pathways. Our results suggest that CRF2 and CRF3 respond to cold via TCS-dependent and TCS-independent pathways and control LR initiation and development, contributing to LR adaptation to cold stress.

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“…Founder cells develop into lateral root primordia and lateral roots, a process modulated by other hormones, environmental signals, and developmental programs. Cytokinins create positional cues for new lateral roots, reducing lateral root formation and ensuring sufficient spacing between two neighboring lateral roots (Laplaze et al, 2007;Šimášková et al, 2015). However, the levels of root cytokinins under standard growth conditions are too high for optimal root growth, as increased root size might help the plant to absorb more water and improve nutrient acquisition.…”

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confidence: 99%