The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression

Garay‐Arroyo, Adriana; Ortiz-Moreno, Enrique; Sánchez, María de la Paz; Murphy, Angus S.; García‐Ponce, Berenice; Marsch-Martínez, Nayelli; Folter, Stefan de; Corvera-Poiré, Adriana; Jaimes-Miranda, Fabiola; Pacheco-Escobedo, Mario A; Dubrovsky, Joseph G.; Pelaz, Soraya; Álvarez-Buylla, Elena

doi:10.1038/emboj.2013.216

Cited by 85 publications

(80 citation statements)

References 74 publications

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“…MADS-domain transcription factors have been shown to be key regulators of plant development (Alvarez-Buylla et al, 2000a;Messenguy and Dubois, 2003;Smaczniak et al, 2012), but their role in modulating cell proliferation and differentiation has not been fully addressed. In previous studies we showed that XAANTAL1 (XAL1/AGL12) and XAANTAL2 (XAL2/AGL14) two MADS-box factors, are necessary for normal root development and cell proliferation control (Tapia-Lopez et al, 2008;Garay-Arroyo et al, 2013). xal1 mutants have shorter roots than wild-type plants with fewer meristematic cells and longer cell-cycle duration, resulting in a diminished cell production rate.…”

Section: Introductionmentioning

confidence: 99%

The MADS-boxXAANTAL1increases proliferation at the Arabidopsis root stem-cell niche and participates in transition to differentiation by regulating cell-cycle components

García-Cruz

García‐Ponce

Garay‐Arroyo

et al. 2016

Ann Bot

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Background Morphogenesis depends on the concerted modulation of cell proliferation and differentiation. Such modulation is dynamically adjusted in response to various external and internal signals via complex transcriptional regulatory networks that mediate between such signals and regulation of cell-cycle and cellular responses (proliferation, growth, differentiation). In plants, which are sessile, the proliferation/differentiation balance is plastically adjusted during their life cycle and transcriptional networks are important in this process. MADS-box genes are key developmental regulators in eukaryotes, but their role in cell proliferation and differentiation modulation in plants remains poorly studied.Methods We characterize the XAL1 loss-of-function xal1-2 allele and overexpression lines using quantitative cellular and cytometry analyses to explore its role in cell cycle, proliferation, stem-cell patterning and transition to differentiation. We used quantitative PCR and cellular markers to explore if XAL1 regulates cell-cycle components and PLETHORA1 (PLT1) gene expression, as well as confocal microscopy to analyse stem-cell niche organization.Key Results We previously showed that XAANTAL1 (XAL1/AGL12) is necessary for Arabidopsis root development as a promoter of cell proliferation in the root apical meristem. Here, we demonstrate that XAL1 positively regulates the expression of PLT1 and important components of the cell cycle: CYCD3;1, CYCA2;3, CYCB1;1, CDKB1;1 and CDT1a. In addition, we show that xal1-2 mutant plants have a premature transition to differentiation with root hairs appearing closer to the root tip, while endoreplication in these plants is partially compromised. Coincidently, the final size of cortex cells in the mutant is shorter than wild-type cells. Finally, XAL1 overexpression-lines corroborate that this transcription factor is able to promote cell proliferation at the stem-cell niche.Conclusion XAL1 seems to be an important component of the networks that modulate cell proliferation/differentiation transition and stem-cell proliferation during Arabidopsis root development; it also regulates several cell-cycle components.

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Section: Introductionmentioning

confidence: 99%

The MADS-boxXAANTAL1increases proliferation at the Arabidopsis root stem-cell niche and participates in transition to differentiation by regulating cell-cycle components

García-Cruz

García‐Ponce

Garay‐Arroyo

et al. 2016

Ann Bot

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“…Root thickness was measured at the level corresponding to the PD/TD boundary for cortex determined by experienced biologists, which implies a subjective method, abbreviated here as the ExpBiol method. The PD/TD boundary determined by an ExpBiol method was defined for epidermis and cortex, arbitrarily based on relative changes in cell lengths or internuclear distances along the root, similar to other studies (Rost and Baum, 1988;Dubrovsky, 1997;Dubrovsky et al, 1998a, b;Tapia-Lopez et al, 2008;Garay-Arroyo et al, 2013).…”

Section: Quantitative Analysismentioning

confidence: 99%

“…The PD/TD boundary has been determined at a point from the QC where, in the shootward direction, cell length or inter-nuclear distance increases significantly and where a cell becomes longer than the average cell length within the PD (Dubrovsky, 1997;Dubrovsky et al, 1998a, b;TapiaLopez et al, 2008;Garay-Arroyo et al, 2013). Blind experiments to determine this boundary on the same roots by different biologists experienced in this technique (ExpBiol) gave similar results, but students or biologists that are inexperienced in this analysis obtained contrasting results (V.B.I., P.D.…”

Section: Determination Of the Pd/td Boundary By The Msc Approach Coinmentioning

confidence: 99%

“…Comparisons between different experimental conditions require approaches that enable accurate evaluations of the size and number of cells within the RAM or its PD. This is generally done in the cortex cell layer (Casamitjana-Martınez et al, 2003;Dello Ioio et al, 2007;Tsukagoshi et al, 2010;Zhou et al, 2011;Garay-Arroyo et al, 2013). However, the lack of objective criteria and subjectivity in identifying the boundaries between root growth zones and domains indicates the need for development of new approaches.…”

Section: Introductionmentioning

confidence: 99%

“…Because of this, the PD/ TD boundary can only be approximated with a certain error, which should be estimated (Ivanov and Dubrovsky, 2013). The position of this boundary can be determined as the point where average cell length along the RAM has slightly increased, or where the distances between nuclei in neighbouring cells along a cell file become greater than the diameter of the nuclei (Rost and Baum, 1988;Dubrovsky et al, 1998a, b;Garay-Arroyo et al, 2013). It is also possible to locate the beginning of the TD as the position where the mitotic index sharply decreases for the tissue under consideration (Ivanov and Dubrovsky, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Pacheco-Escobedo

Ivanov

Ransom-Rodríguez

et al. 2016

Ann Bot

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Background and Aims The Arabidopsis thaliana root is a key experimental system in developmental biology. Despite its importance, we are still lacking an objective and broadly applicable approach for identification of number and position of developmental domains or zones along the longitudinal axis of the root apex or boundaries between them, which is essential for understanding the mechanisms underlying cell proliferation, elongation and differentiation dynamics during root development.Methods We used a statistics approach, the multiple structural change algorithm (MSC), for estimating the number and position of developmental transitions in the growing portion of the root apex. Once the positions of the transitions between domains and zones were determined, linear models were used to estimate the critical size of dividing cells (L critD ) and other parameters.Key Results The MSC approach enabled identification of three discrete regions in the growing parts of the root that correspond to the proliferation domain (PD), the transition domain (TD) and the elongation zone (EZ). Simultaneous application of the MSC approach and G2-to-M transition (CycB1;1DB:GFP) and endoreduplication (pCCS52A1:GUS) molecular markers confirmed the presence and position of the TD. We also found that the MADS-box gene XAANTAL1 (XAL1) is required for the wild-type (wt) PD increase in length during the first 2 weeks of growth. Contrary to wt, in the xal1 loss-of-function mutant the increase and acceleration of root growth were not detected. We also found alterations in L critD in xal1 compared with wt, which was associated with longer cell cycle duration in the mutant.Conclusions The MSC approach is a useful, objective and versatile tool for identification of the PD, TD and EZ and boundaries between them in the root apices and can be used for the phenotyping of different genetic backgrounds, experimental treatments or developmental changes within a genotype. The tool is publicly available at www.ibiologia.com.mx/MSC_analysis.

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Pericycle

Dubrovsky

Rost

2023

Encyclopedia of Life Sciences

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Pericycle is a primary tissue of plant roots with meristematic properties and is the site for the initiation of lateral roots and two secondary meristems, the vascular cambium and phellogen (cork cambium). Pericycle pluripotent cell properties are also revealed during cultivation of root explants in shoot regeneration media. In this article, the characteristics of the pericycle related to each of its functions are reviewed. During lateral root development, five important and coordinated events take place in the pericycle: founder cell identity acquisition, cell division competence, asymmetric cell division, new organ growth axis establishment and lateral inhibition. Cellular and molecular bases of these processes as well as transcriptomic insights in pericycle cell identity are discussed. Cell cycle and related genetic control in pericycle development are also addressed. Cellular and molecular bases of participation of pericycle in the formation of lateral meristems, vascular cambium and phellogen (cork cambium), differences among eudicots and monocots in pericycle development, as well as participation of pericycle in loading of mineral nutrients and unloading of organic compounds are also reviewed. Key Concepts The pericycle is a primary tissue with pluripotent properties that participates in lateral root (LR) formation. In eudicots, it also gives rise to two lateral meristems: vascular cambium and cork cambium (phellogen). Pericycle is typical of plant roots and is the most external cell layer (or layers) of the vascular cylinder. In other plant organs, pericycle or pericycle‐like cell layers can also be present depending on taxon. Outside the root apical meristem, in the root differentiation zone of eudicots, the xylem pole pericycle (XPP) maintains its proliferation activity. Due to its proliferation activity, pericycle possesses high regenerative properties involved in regeneration of shoots from roots. The XPP and phloem pole pericycle (PPP) are characterised by distinct transcriptomic profiles related to their adjacent vascular tissues. Pericycle cells committed for LR development in monocots and eudicots retain the common features related to cell cycle, active auxin synthesis, transport and signalling, and responsiveness to nitrates. LR formation starts from pericycle founder cell specification which is auxin dependent and implies drastic developmental changes in genetic programs involved in asymmetric cell division, new organ growth axis establishment and lateral inhibition. The first founder cell specification is followed by the recruitment of neighbouring pericycle cells that leads to the formation of a morphogenetic field of founder cells giving rise to a LR. The transition from primary to secondary growth starts in the pericycle and procambium and leads to the formation of vascular cambium and phellogen which are coordinated processes dependent on auxin and cytokinin. Pericycle maintains high metabolic activity and participates in loading phloem and xylem and in unloading phloem and thus is involved in shoot‐to‐root and root‐to‐shoot long‐distance transport.

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The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression

Cited by 85 publications

References 74 publications

The MADS-boxXAANTAL1increases proliferation at the Arabidopsis root stem-cell niche and participates in transition to differentiation by regulating cell-cycle components

The MADS-boxXAANTAL1increases proliferation at the Arabidopsis root stem-cell niche and participates in transition to differentiation by regulating cell-cycle components

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Pericycle

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