Auxin transport and activity regulate stomatal patterning and development

Le, Jie; Liu, Xuguang; Yang, Kezhen; Chen, Xiaolan; Zou, Junjie; Wang, Hongzhe; Wang, Ming; Vanneste, Steffen; Morita, Miyo Terao; Tasaka, Masao; Ding, Zhaojun; Friml, Jiřı́; Beeckman, Tom; Sack, Fred D.

doi:10.1038/ncomms4090

Cited by 123 publications

(131 citation statements)

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“…Moreover, we have placed AXR3 within the genetic signalling network that regulates stomatal development in response to intrinsic and external signals. Taken together with a recent report demonstrating the important role of polar auxin transport and auxin distribution in stomatal patterning of light-grown seedlings (Le et al, 2014), our results support the notion that auxin is a negative regulator of stomatal differentiation.…”

Section: Discussionsupporting

confidence: 90%

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Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins

et al. 2014

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Stomatal development is tightly regulated through internal and external factors that are integrated by a complex signalling network. Light represents an external factor that strongly promotes stomata formation. Here, we show that auxin-resistant aux/iaa mutants, e.g. axr3-1, exhibit a de-repression of stomata differentiation in dark-grown seedlings. The higher stomatal index in dark-grown axr3-1 mutants when compared with the wild type is due to increased cell division in the stomatal lineage. Excessive stomata in dark-grown seedlings were also observed in mutants defective in auxin biosynthesis or auxin perception and in seedlings treated with the polar auxin transport inhibitor NPA. Consistent with these findings, exogenous auxin repressed stomata formation in light-grown seedlings. Taken together, these results indicate that auxin is a negative regulator of stomatal development in dark-grown seedlings. Epistasis analysis revealed that axr3-1 acts genetically upstream of the bHLH transcription factors SPCH, MUTE and FAMA, as well as the YDA MAP kinase cascade, but in parallel with the repressor of photomorphogenesis COP1 and the receptor-like protein TMM. The effect of exogenous auxin required the ER family of leucine-rich repeat receptor-like kinases, suggesting that auxin acts at least in part through the ER family. Expression of axr3-1 in the stomatal lineage was insufficient to alter the stomatal index, implying that cell-cell communication is necessary to mediate the effect of auxin. In summary, our results show that auxin signalling contributes to the suppression of stomatal differentiation observed in dark-grown seedlings.

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Section: Discussionsupporting

confidence: 90%

“…It has been recently shown that polar auxin transport is crucial for maintaining the one-cell-spacing rule in stomatal patterning. High auxin activity has been observed during unequal cell divisions, whereas a decrease in auxin activity promotes GMC fate and its subsequent equal division into two guard cells (Le et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins

et al. 2014

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“…This work advances our knowledge about auxin's role in stomatal development and the underlying molecular mechanism. To note, it is shown in this recent work that exogenously applied auxin fails to lead to pronounced stomatal development phenotype, based on the production of stomatal clusters but not SMI (59). In the present study, exogenous 2,4-D application results in a significant decrease in SMI (Fig.…”

Section: Discussionsupporting

confidence: 62%

“…During the revision of our paper, a study reports that altered auxin transport, made either by mutation of auxin efflux transporters or by inhibition of auxin transport with inhibitors, affects stomatal patterning (59). However, the precise physiological role of auxin in the regulation of stomatal development, the regulatory signaling pathway, as well as the underlying molecular mechanisms have basically not been revealed.…”

Section: Discussionmentioning

confidence: 99%

Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll

Zhang

et al. 2014

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

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Plants, as sessile organisms, must coordinate various physiological processes to adapt to ever-changing surrounding environments. Stomata, the epidermal pores facilitating gas and water exchange, play important roles in optimizing photosynthetic efficiency and adaptability. Stomatal development is under the control of an intrinsic program mediated by a secretory peptide gene familynamely, EPIDERMAL PATTERNING FACTOR, including positively acting STOMAGEN/EPFL9. The phytohormone brassinosteroids and environment factor light also control stomatal production. However, whether auxin regulates stomatal development and whether peptide signaling is coordinated with auxin signaling in the regulation of stomatal development remain largely unknown. Here we show that auxin negatively regulates stomatal development through MONOPTEROS (also known as ARF5) repression of the mobile peptide gene STOMAGEN in mesophyll. Through physiological, genetic, transgenic, biochemical, and molecular analyses, we demonstrate that auxin inhibits stomatal development through the nuclear receptor TIR1/AFB-mediated signaling, and that MONOPTEROS directly binds to the STOMAGEN promoter to suppress its expression in mesophyll and inhibit stomatal development. Our results provide a paradigm of cross-talk between phytohormone auxin and peptide signaling in the regulation of stomatal production.A uxin is the first identified phytohormone, which exerts multifaceted influences on plant growth and development, such as embryonic root initiation (1, 2), shoot apical meristem function (3), and floral primordia initiation (4). As a "molecular glue," auxin facilitates the formation of its coreceptor complexes comprising F-box proteins (TIR1/AFBs) and AUXIN/INDOLE-3-ACETIC ACID proteins (AUX/IAAs), and subsequent AUX/ IAAs ubiquitination and degradation by 26S proteasome, thus releasing auxin response factors (ARFs) from AUX/IAAs repression to regulate auxin-responsive gene expression by either activation or repression (2, 3, 5-11). Although many physiologic processes are reported to be regulated by auxin (1-4, 6, 12), the full understanding of the functions of this versatile phytohormone has not been reached.Stomata, the pores flanked by a pair of guard cells, mainly constitute the epidermis of plant leaves together with trichomes and neighboring pavement cells that separate stomata to maintain the one-cell spacing rule (13,14). As a gas and water passage between external environment and internal plant tissue, stomata play important roles in photosynthesis and global carbon and water circulation (15). Stomatal generation undergoes several stages, including meristemoid mother cell, meristemoid, guard mother cell, and guard cells, which is modulated by an intrinsic program (14) mainly involving putative peptide ligands [EPI-DERMAL PATTERNING FACTOR (EPF) family] (16-20), membrane proteins (receptor-like protein TMM and receptorlike kinase ERECTA family) (21-23), MAPK cascades (protein kinase YDA, MKK4/5/7/9, and MPK3/6) (24-26), and transcription factors (bHLH...

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“…In Nicotiana, auxin aslo regulate cell division, polarity formation, seed germination as well as stomata movement [8,9,10]. Recently Le et al reported auxin transport and signaling regulate stomatal patterning and development in Arabidopsis [11], But it remains unknown whether this regulation mechanism is also existed in other species. Use Nicotiana as subject, effect of auxin transport inhibitor NAP [12,13] and BFA [14,15] on its stomatal developement was analyzed to compare with Arabidopsis.…”

Section: Introductionmentioning

confidence: 99%

Difference of auxin transport inhibitor treatment on several development processes between Arabidopsis and Nicotiana seedlings

Zhou¹,

Chen²,

Chen³

et al. 2016

Proceedings of the 2016 International Conference on Civil, Structure and Environmental Engineering

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Abstract. Auxin transport and signaling enforce stomatal patterning as well as the size of their stem cell compartment in Arabidopsis. But it remains unknown whether this regulation is also existed in other species. We use Nicotiana as an example to analysis the function of auxin transport inhibitor NAP and BFA on its stomatal developement on the epidermis of cotyledon taking Arabidopsis as control. Here we report that there is an inter-specific difference between Nicotiana and Arabidopsis under exogerous auxin inhibitors (NPA and BFA) treatment in stomatal development. No stomatal development defect can be detected in Nicotiana treated with NPA and BFA under the same concentration which can induce patterning and morphogenesis abnormality of stoma in Arabidopsis.

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Auxin transport and activity regulate stomatal patterning and development

Cited by 123 publications

References 45 publications

Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins

Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins

Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll

Difference of auxin transport inhibitor treatment on several development processes between Arabidopsis and Nicotiana seedlings

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