Elsevier

Journal of Plant Physiology

Volume 201, 20 August 2016, Pages 79-84
Journal of Plant Physiology

Short communication
Increased STM expression is associated with drought tolerance in Arabidopsis

https://doi.org/10.1016/j.jplph.2016.07.002Get rights and content

Abstract

In higher plants, shoot apical meristem (SAM) maintains cell division activity in order to give rise to aerial plant organs. Several lines of evidence have suggested that plants ensure stem cell proliferation activity in response to various external stimuli, thereby contributing to plant adaptation and fitness. Here, we report that the abscisic acid (ABA)-inducible R2R3-type MYB96 transcription factor regulates transcript accumulation of SHOOT MERISTEMLESS (STM) possibly to contribute to plant adaptation to environmental stress. STM was up-regulated in MYB96-overexpressing activation-tagging myb96-ox plants, but down-regulated in MYB96-deficient myb96-1 mutant plants, even in the presence of ABA. Notably, the MYB96 transcription factor bound directly to the STM promoter. In addition, consistent with the role of MYB96 in drought tolerance, transgenic plants overexpressing STM (35S:STM-MYC) were more tolerant to drought stress. These observations suggest that the MYB96-STM module contributes to enhancing plant tolerance to drought stress.

Introduction

The SAM retains an indeterminate pluripotent nature in order to give rise to the aerial parts of plants. New organs are differentiated in the peripheral zone (PZ) (Dodsworth, 2009). The cell population in the PZ is maintained by continuous recruitment of stem cells from the central zone (CZ) (Gallois et al., 2002). The balance between the rate of cell proliferation and differentiation is crucial for the ordered transition of cells.

A well-known signaling mechanism in the stem cell niche is the negative feedback regulation between CLAVATA3 (CLV3) and WUSCHEL (WUS). The homeodomain transcription factor WUS activates CLV3 though direct binding to its promoter and promotes stem cell division (Yadav et al., 2011). The mature 12-amino-acid CLV3 peptide perceived by CLV receptor complexes, including CLV1, CLV2, SUPPRESSOR OF LLP1-2 (SOL2)/CORYNE (CRN) and RECEPTOR LIKE PROTEIN KINASE 2 (RPK2)/TOADSTOOL 2 (TOAD2), represses WUS expression. The CLV3-WUS module is necessary to maintain the pool of stem cells in the CZ of the meristem (Brand et al., 2000, Schoof et al., 2000).

In addition, the class I KNOTTED1-like homeobox (KNOX) genes constitute another important genetic pathway that determines stem cell establishment and maintenance, as well as prevents organ differentiation. In particular, the STM gene is mainly expressed in both the CZ and PZ of the meristem and maintains the cells in an undifferentiated state (Barton and Poethig, 1993, Clark et al., 1996, Gallois et al., 2002, Long et al., 1996). The other SAM-expressed class I KNOX members, including BREVIPEDICELLUS (BP)/KNOTTED-LIKE GENE FROM ARABIDOPSIS THALIANA 1 (KNAT1), KNAT2, and KNAT6, have functions partially redundant with STM in maintaining indeterminate stem cell fate by modulating hormone metabolism (Hay et al., 2002, Jasinski et al., 2005, Yanai et al., 2005).

Plants have evolved elaborate protective mechanisms to deal with environmental challenges, such as temperature extremes, water deficit, and high salinity. Upon exposure to abiotic stresses, they stimulate altered shoot and root development, biosynthesis of osmoprotectants, reprogramming of primary and secondary metabolite accumulation, and reestablishment of hormone homeostasis (Kido et al., 2013, Peleg and Blumwald, 2011, Ramakrishna and Ravishankar, 2011). In addition, several recent studies have supported the idea that plants also require stem cell proliferation activity to attain developmental plasticity, and thus to overcome their sessile nature under environmentally unfavorable conditions. In support of this, abiotic stress-experienced cells show a stem cell-like state (Grafi et al., 2011a, Grafi et al., 2011b). Furthermore, the transcriptome of stress-experienced cells largely overlaps with that of stem cells or dedifferentiated cells (Grafi et al., 2011b). Maintenance of the undifferentiated state might enable plants to acquire a new cell fate with better fitness to environmental disadvantages (Shoshani and Zipori, 2011). However, it is unclear how environmental fluctuation affects meristem proliferative activity in plants.

In this study, we report that the R2R3-type MYB96 transcription factor, a central ABA signaling mediator, establishes possible links between the STM expression and drought tolerance. The MYB96 transcription factor binds to the STM promoter and activates its expression under drought conditions. Consistent with this, STM-overexpressing transgenic plants showed enhanced tolerance to drought stress. These observations provide novel insight into how plants ensure indeterminate cell division to enhance their adaptation capability under stressful conditions.

Section snippets

Plant material and growth conditions

Arabidopsis thaliana (Columbia-0 ecotype) was used for all experiments described, unless specified otherwise. Plants were grown under long day conditions (LDs; a 16-h light/8-h dark cycle) with cool white fluorescent light (100 μmol photons m−2 s−1) at 22 °C. The myb96-ox and myb96-1 mutants were previously reported (Seo et al., 2009). To produce transgenic plants overexpressing the STM and WUS genes, the full-length cDNAs were subcloned into the binary pBA002 vector under the control of the

Regulation of STM expression by MYB96

We previously reported that MYB96 regulates a variety of physiological processes under drought conditions, and consistent with its diverse roles, the MYB96-overexpressing activation-tagging myb96-ox mutant show pleiotropic developmental phenotypes, including dwarfism, reduced height, smaller and curled leaves, and delayed flowering (Seo et al., 2009, Seo et al., 2011, Seo and Park, 2010). In particular, what we focused on in this study was that myb96-ox plants have altered phyllotaxis and a

Environmental stress regulation of STM expression

Two proteins, STM and WUS, are implicated in the maintenance of undifferentiated cells in the SAM, and consistent with their functional overlap, their functional interactions have been previously demonstrated (Lenhard et al., 2002). Coexpression of the two genes results in synergistic effects on stem cell proliferation (Lenhard et al., 2002). In addition, ectopic expression of WUS partly compensates for STM function. It is likely that the pathways regulated by STM and WUS are mutually required

Author contributions

P.J.S. conceived and designed the experiments. P.J.S wrote the paper with the help of H.G.L. H.G.L. and Y.R.C conducted the experiments.

Acknowledgements

This work was supported by the Global Research Network (NRF-2014S1A2A2028392) program provided by the National Research Foundation of Korea and by the Next-Generation BioGreen 21 Program (PJ01109001) provided by the Rural Development Administration.

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