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, 146 (3), 1182-92

An AGAMOUS-related MADS-box Gene, XAL1 (AGL12), Regulates Root Meristem Cell Proliferation and Flowering Transition in Arabidopsis

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An AGAMOUS-related MADS-box Gene, XAL1 (AGL12), Regulates Root Meristem Cell Proliferation and Flowering Transition in Arabidopsis

Rosalinda Tapia-López et al. Plant Physiol.

Abstract

MADS-box genes are key components of the networks that control the transition to flowering and flower development, but their role in vegetative development is poorly understood. This article shows that the sister gene of the AGAMOUS (AG) clade, AGL12, has an important role in root development as well as in flowering transition. We isolated three mutant alleles for AGL12, which is renamed here as XAANTAL1 (XAL1): Two alleles, xal1-1 and xal1-2, are in Columbia ecotype and xal1-3 is in Landsberg erecta ecotype. All alleles have a short-root phenotype with a smaller meristem, lower rate of cell production, and abnormal root apical meristem organization. Interestingly, we also encountered a significantly longer cell cycle in the strongest xal1 alleles with respect to wild-type plants. Expression analyses confirmed the presence of XAL1 transcripts in roots, particularly in the phloem. Moreover, XAL1beta-glucuronidase expression was specifically up-regulated by auxins in this tissue. In addition, mRNA in situ hybridization showed that XAL1 transcripts were also found in leaves and floral meristems of wild-type plants. This expression correlates with the late-flowering phenotypes of the xal1 mutants grown under long days. Transcript expression analysis suggests that XAL1 is an upstream regulator of SOC, FLOWERING LOCUS T, and LFY. We propose that XAL1 may have similar roles in both root and aerial meristems that could explain the xal1 late-flowering phenotype.

Figures

Figure 1.
Figure 1.
XAL1 phylogeny and seedling mutant phenotypes. A, Bayesian reconstruction of the phylogenetic relationships among selected type II Arabidopsis MADS-box genes, with XAL1 position indicated by an arrow. Numbers under the branches represent Bayesian posterior probability and can be interpreted as a measure of clade statistical support. B, Seedlings phenotype. Ten-day-old wild-type (Col-0 and Ler ecotypes) and xal1-1, xal1-2, and xal1-3 alleles were grown on vertical 0.2× Murashige and Skoog plates. On the top, XAL1 gene schematic model with the sites of transposon or T-DNA insertions are shown. C, XAL1 expression in root tissue from 14-d-old seedlings. Total RNA of both wild-type ecotypes and xal1 alleles were subject to northern-blot hybridization (10 μg/lane; top) and semiquantitative RT-PCR. 28S and TUBULIN were used as internal load controls, respectively.
Figure 2.
Figure 2.
Root phenotype of xal1 mutants. A, Open meristem organization in xal1 alleles. Seven-day-old seedlings were stained with propidium iodide and analyzed by confocal microscopy. QC cells of wild type (arrows) and mutants (arrowhead) of representative phenotypes are shown (bar = 10 μm). Black-and-white zoom picture of xal1-2 is shown to highlight abnormal periclinal divisions at the QC and deformed columella cells. B, Root cellular parameter analyses. Meristem length of 20 independent plants was measured from Col-0 and Ler wild-type plants and xal1-1, xal1-2, and xal1-3 alleles (1-1, 1-2, 1-3). Cell production rate, cell-cycle duration, and fully elongated cell length were obtained as described in “Materials and Methods.” Bars = ses, calculated with JMP, version 5.1.1, statistical package (see data in Supplemental Table S1).
Figure 3.
Figure 3.
XAL1 phloem expression is induced by auxins. A, Confocal image of an XAL1GFP line taken at the protophloem plane, counterstained with propidium iodide. B, Transverse section of root XAL1GUS line after GUS staining, counterstained with ruthenium red. C and D, XAL1GUS expression in two different stages of lateral root development. E, Lateral root length along the primary root axis of the wild type (wt) and xal1-1 allele (n = 15 plants; bars = ses). F, XAL1GUS expression without (−IAA) and with (+IAA 2 μm). G, IAA-induced phloem GUS activity driven by the XAL1 promoter (left) compared to the broad expression of the DR5GUS line (right), after they were both treated with IAA (2 μm).
Figure 4.
Figure 4.
Flowering phenotype of xal1-1 and xal1-2 mutants and XAL1 role in the photoperiod pathway. A, Late-flowering transition phenotype of the xal1-1 mutant compared to wild-type plants. Both plants were 32 d old. B, XAL1 mRNA in situ hybridizations. XAL1 expression (arrows) in vascular tissue (v) of a 20 d after planting (DAP) vegetative shoot transverse section (top); in the inflorescence meristem (IM) longitudinal section (middle); and in the gynoecium (g) and anthers of a floral meristem (bottom). C, GUS expression in a floral bud longitudinal section of the XAL1GUS line. Strong GUS staining corresponds to the nectaries (n). D, Late-flowering phenotype of xal1 mutants. Bolting time scored by DAP at bolting (see data for LD; Table I) in black bars and total rosette leaf number (RLN) in white bars of xal1-1 and xal1-2 alleles compared to wild-type plants (wt). E, Comparative transcript accumulation of genes that participate in the photoperiod and integrative flowering pathways. Gene expression levels were analyzed in the shoots of 14-d-old seedlings of wild type and xal1 mutants by RT-PCR. TUBULIN was included as a constitutive control. A to E, Plants were grown under LD photoperiods.
Figure 5.
Figure 5.
Model for the role of XAL1 in root and shoot development. The MADS-box gene, XAL1, might mediate auxin participation in the proliferation of the root meristematic cells and the shoot meristem. In the root, XAL1 may also be implicated in cell elongation because the xal1-2 allele has smaller cells than wild type. Auxin may participate in the shoot meristem transition to flowering, mediating light induction of XAL1, which in turn may be an important promoter of downstream regulators in the photoperiod pathway. CO also induces XAL1 expression probably by the classical photoperiod pathway. Solid arrows indicate direct proved regulation and dashed arrows suggest direct/indirect regulation.

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