Warm Temperature Promotes Shoot Regeneration inArabidopsis thaliana
Alice LambolezAyako KawamuraTatsuya TakahashiBart RymenAkira IwaseDavid S. FaveroMomoko IkeuchiTakamasa SuzukiSandra CortijoKatja E. JaegerPhilip A. WiggeKeiko Sugimoto
21
Citation
95
Reference
10
Related Paper
Citation Trend
Abstract:
Many plants are able to regenerate upon cutting, and this process can be enhanced in vitro by incubating explants on hormone-supplemented media. While such protocols have been used for decades, little is known about the molecular details of how incubation conditions influence their efficiency. In this study, we find that warm temperature promotes both callus formation and shoot regeneration in Arabidopsis thaliana. We show that such an increase in shoot regenerative capacity at higher temperatures correlates with the enhanced expression of several regeneration-associated genes, such as CUP-SHAPED COTYLEDON 1 (CUC1) encoding a transcription factor involved in shoot meristem formation and YUCCAs (YUCs) encoding auxin biosynthesis enzymes. ChIP-sequencing analyses further reveal that histone variant H2A.Z is enriched on these loci at 17°C, while its occupancy is reduced by an increase in ambient temperature to 27°C. Moreover, we provide genetic evidence to demonstrate that H2A.Z acts as a repressor of de novo shoot organogenesis since H2A.Z-depleted mutants display enhanced shoot regeneration. This study thus uncovers a new chromatin-based mechanism that influences hormone-induced regeneration and additionally highlights incubation temperature as a key parameter for optimizing in vitro tissue culture.Keywords:
Organogenesis
Callus
Plant hormone
Cutting
Epidermis (zoology)
Plant Physiology
Cite
Citations (144)
Plant hormones regulate many aspects of plant growth and development. Both auxin and cytokinin have been known for a long time to act either synergistically or antagonistically to control several significant developmental processes, such as the formation and maintenance of meristem. Over the past few years, exciting progress has been made to reveal the molecular mechanisms underlying the auxin-cytokinin action and interaction. In this review, we shall briefly discuss the major progress made in auxin and cytokinin biosynthesis, auxin transport, and auxin and cytokinin signaling. The frameworks for the complicated interaction of these two hormones in the control of shoot apical meristem and root apical meristem formation as well as their roles in in vitro organ regeneration are the major focus of this review.
Plant hormone
Cite
Citations (575)
Organogenesis
Developmental Biology
Cite
Citations (3)
Like animals, the mature plant body develops via successive sets of instructions that determine cell fate, patterning, and organogenesis. In the coordination of various developmental programs, several plant hormones play decisive roles, among which auxin is the best-documented hormonal signal. Despite the broad range of processes influenced by auxin, how such a single signaling molecule can be translated into a multitude of distinct responses remains unclear. In Arabidopsis thaliana , lateral root development is a classic example of a developmental process that is controlled by auxin at multiple stages. Therefore, we used lateral root formation as a model system to gain insight into the multifunctionality of auxin. We were able to demonstrate the complementary and sequential action of two discrete auxin response modules, the previously described SOLITARY ROOT/INDOLE-3-ACETIC ACID (IAA)14-AUXIN REPONSE FACTOR (ARF)7-ARF19–dependent lateral root initiation module and the successive BODENLOS/IAA12-MONOPTEROS/ARF5–dependent module, both of which are required for proper organogenesis. The genetic framework in which two successive auxin response modules control early steps of a developmental process adds an extra dimension to the complexity of auxin’s action.
Organogenesis
Plant hormone
Lateral root
Developmental Biology
Cite
Citations (283)
Summary The organization of the root meristem is maintained by a complex interplay between plant hormones signaling pathways that both interpret and determine their accumulation and distribution. Brassinosteroids (BR) and auxin signaling pathways control the number of meristematic cells in the Arabidopsis root, via an interaction that appears to involve contradicting molecular outcomes, with BR promoting auxin signaling input but also repressing its output. However, whether this seemingly incoherent effect is significant for meristem function is unclear. Here, we established that a dual effect of BR on auxin, with BR simultaneously promoting auxin biosynthesis and repressing auxin transcriptional output, is essential for meristem maintenance. Blocking BR-induced auxin synthesis resulted in rapid BR-mediated meristem loss. Conversely, plants with reduced BR levels were resistant to loss of auxin biosynthesis and these meristems maintained their normal morphology despite a 10-fold decrease in auxin levels. In agreement, injured root meristems which rely solely on local auxin synthesis, regenerated when both auxin and BR synthesis were inhibited. Use of BIN2 as a tool to selectively inhibit BR signaling, revealed meristems with distinct phenotypes depending on the perturbed tissue; meristem reminiscent of BR-deficient mutants or of high BR exposure. This enabled mapping BR-auxin interactions to the outer epidermis and lateral root cap tissues, and demonstrated the essentiality of BR signaling in these tissues for meristem maintenance. BR activity in internal tissues however, proved necessary to control BR homeostasis. Together, we demonstrate a basis for inter-tissue coordination and how a critical ratio between these hormones determines the meristematic state.
Brassinosteroid
Plant hormone
Cite
Citations (2)
The primary architecture of the aerial part of plants is controlled by the shoot apical meristem, a specialized tissue containing a stem cell niche. The iterative generation of new aerial organs, (leaves, lateral inflorescences, and flowers) at the meristem follows regular patterns, called phyllotaxis. Phyllotaxis has long been proposed to self‐organize from the combined action of growth and of inhibitory fields blocking organogenesis in the vicinity of existing organs in the meristem. In this review, we will highlight how a combination of mathematical/computational modeling and experimental biology has demonstrated that the spatiotemporal distribution of the plant hormone auxin controls both organogenesis and the establishment of inhibitory fields. We will discuss recent advances showing that auxin likely acts through a combination of biochemical and mechanical regulatory mechanisms that control not only the pattern of organogenesis in the meristem but also postmeristematic growth, to shape the shoot. WIREs Dev Biol 2016, 5:460–473. doi: 10.1002/wdev.231 This article is categorized under: Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition Gene Expression and Transcriptional Hierarchies > Quantitative Methods and Models Plant Development > Inflorescence, Flower, and Fruit Development
Phyllotaxis
Organogenesis
Developmental Biology
Cite
Citations (23)
The Arabidopsis root is a dynamic system where the interaction between different plant hormones controls root meristem activity and, thus, organ growth. In the root, a characteristic graded distribution of the hormone auxin provides positional information, coordinating the proliferating and differentiating cell status. The hormone cytokinin shapes this gradient by positioning an auxin minimum in the last meristematic cells. This auxin minimum triggers a cell developmental switch necessary to start the differentiation program, thus, regulating the root meristem size. To position the auxin minimum, cytokinin promotes the expression of the IAA-amido synthase group II gene GH3.17, which conjugates auxin with amino acids, in the most external layer of the root, the lateral root cap tissue. Since additional GH3 genes are expressed in the root, we questioned whether cytokinin to position the auxin minimum also operates via different GH3 genes. Here, we show that cytokinin regulates meristem size by activating the expression of GH3.5 and GH3.6 genes, in addition to GH3.17. Thus, cytokinin activity provides a robust control of auxin activity in the entire organ necessary to regulate root growth.
Lateral root
Plant hormone
Cite
Citations (42)
AbstractCytokinin and auxin antagonistically affect cell proliferation and differentiation and thus regulate root meristem size by influencing the abundance of SHORT HYPOCOTYL2 (SHY2/IAA3). SHY2 affects auxin distribution in the root meristem by repressing the auxin-inducible expression of PIN-FORMED (PIN) auxin transport genes. The PLETHORA (PLT1/2) genes influence root meristem growth by promoting stem cells and transit-amplifying cells. However, the factors connecting cytokinin, auxin, SHY2 and PLT1/2 are largely unknown. In a recent study, we have shown that the DA1-related protein 2 (DAR2) acts downstream of cytokinin and SHY2 but upstream of PLT1/2 to affect root meristem size. Here, we discuss the possible molecular mechanisms by which Arabidopsis DAR2 controls root meristem size.Keywords:: auxincytokininDAR2root meristem sizestem cell niche activityThis article is related to:
Cite
Citations (10)
Growth of the aerial part of the plant is dependent upon the maintenance of the shoot apical meristem (SAM). A balance between the self-renewing stem cells in the central zone (CZ) and organogenesis in the peripheral zone (PZ) is essential for the integrity, function, and maintenance of the SAM. Understanding how the SAM maintains a balance between stem cell perpetuation and organogenesis is a central question in plant biology. Two related BELL1-like homeodomain proteins, PENNYWISE (PNY) and POUND-FOOLISH (PNF), act to specify floral meristems during reproductive development. However, genetic studies also show that PNY and PNF regulate the maintenance of the SAM. To understand the role of PNY and PNF in meristem maintenance, the expression patterns for genes that specifically localize to the peripheral and central regions of the SAM were examined in Arabidopsis (Arabidopsis thaliana). Results from these experiments indicate that the integrity of the CZ is impaired in pny pnf plants, which alters the balance of stem cell renewal and organogenesis. As a result, pools of CZ cells may be allocated into initiating leaf primordia. Consistent with these results, the integrity of the central region of pny pnf SAMs can be partially restored by increasing the size of the CZ. Interestingly, flower specification is also reestablished by augmenting the size of the SAM in pny pnf plants. Taken together, we propose that PNY and PNF act to restrict organogenesis to the PZ by maintaining a boundary between the CZ and PZ.
Organogenesis
Primordium
Cite
Citations (55)
This study investigates the auxin regulation of lateral meristem activation in the gametophytes of the fern Ceratopteris richardii Brongn. Exogenous auxin in the form of α-naphthaleneacetic acid or 2,4,5-trichlorophenoxy-acetic acid repressed the activation of the lateral meristem, and generated a male-like body plan. The auxin antagonist p-chlorophenoxyisobutyric acid reduced activity of both the apical and lateral meristems, and produced a circular-shaped gametophyte. Disrupting auxin transport with 2,3,5-triiodobenzoic acid led to a time lag in lateral meristem activation, while disrupting auxin transport with n-1-naphthylphthalamic acid produced several different body plans generated by the formation of a second lateral meristem. These findings suggest auxin mediates the activation of the lateral meristem and regulates lateral meristem function. In addition, auxin transport may be necessary for communication between the lateral meristem and other regions of the developing gametophyte. Auxin also controls the position of rhizoids produced by the gametophyte, and exogenous auxin interferes with the sexual differentiation of the gametophyte. These results are summarized in a model of how auxin regulates lateral meristem activation and meristem activity during gametophyte development in C. richardii.
Polar auxin transport
Cite
Citations (15)