Lateral Root Primordium Morphogenesis in Angiosperms

Morphogenetic processes are the basis of new organ formation. Lateral roots (LRs) are the building blocks of the root system. After LR initiation and before LR emergence, a new lateral root primordium (LRP) forms. During this period, the organization and functionality of the prospective LR is defined. Thus, proper LRP morphogenesis is a decisive process during root system formation. Most current studies on LRP morphogenesis have been performed in the model species Arabidopsis thaliana; little is known about this process in other angiosperms. To understand LRP morphogenesis from a wider perspective, we review both contemporary and earlier studies. The latter are largely forgotten, and we attempted to integrate them into present-day research. In particular, we consider in detail the participation of parent root tissue in LRP formation, cell proliferation and timing during LRP morphogenesis, and the hormonal and genetic regulation of LRP morphogenesis. Cell type identity acquisition and new stem cell establishement during LRP morphogenesis are also considered. Within each of these facets, unanswered or poorly understood questions are identified to help define future research in the field. Finally, we discuss emerging research avenues and new technologies that could be used to answer the remaining questions in studies of LRP morphogenesis

An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis

11 pages, 5 figures, 1 table.-- PMID: 18203871 [PubMed].-- PMCID: PMC2259045.-- Supplementary information available at: http://www.plantphysiol.org/cgi/content/full/pp.107.108647/DC1MADS-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.This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACYT), México (grant nos. CO1.41848/A–1, CO1.0538/A–1, and CO1.0435.B–1); Dirección General de Asuntos del Personal Académico (DGAPA)-Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT), Universidad Nacional Autónoma de México (UNAM; grant nos. IN230002 and IX207104); and the University of California-MEXUS ECO IE 271 to E.R.A.-B. R.T.-L. was a recipient of CONACYT and DGAPA-PAPIIT-UNAM fellowships (no. IX225304). J.G.D. was supported by DGAPA-PAPIIT-UNAM (grant nos. IN210202 and IN225906) and CONACYT (grant no. 49267).Peer reviewe

The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation

Cyclophilin A is a conserved peptidyl-prolyl cis-trans isomerase (PPIase) best known as the cellular receptor of the immunosuppressant cyclosporine A. Despite significant effort, evidence of developmental functions of cyclophilin A in non-plant systems has remained obscure. Mutations in a tomato (Solanum lycopersicum) cyclophilin A ortholog, DIAGEOTROPICA (DGT), have been shown to abolish the organogenesis of lateral roots; however, a mechanistic explanation of the phenotype is lacking. Here, we show that the dgt mutant lacks auxin maxima relevant to priming and specification of lateral root founder cells. DGT is expressed in shoot and root, and localizes to both the nucleus and cytoplasm during lateral root organogenesis. Mutation of ENTIRE/IAA9, a member of the auxin-responsive Aux/IAA protein family of transcriptional repressors, partially restores the inability of dgt to initiate lateral root primordia but not the primordia outgrowth. By comparison, grafting of a wild-type scion restores the process of lateral root formation, consistent with participation of a mobile signal. Antibodies do not detect movement of the DGT protein into the dgt rootstock; however, experiments with radiolabeled auxin and an auxin-specific microelectrode demonstrate abnormal auxin fluxes. Functional studies of DGT in heterologous yeast and tobacco-leaf auxin-transport systems demonstrate that DGT negatively regulates PIN-FORMED (PIN) auxin efflux transporters by affecting their plasma membrane localization. Studies in tomato support complex effects of the dgt mutation on PIN expression level, expression domain and plasma membrane localization. Our data demonstrate that DGT regulates auxin transport in lateral root formation

Unique cellular organization in the oldest root meristem

Roots and shoots of plant bodies develop from meristems—cell populations that self-renew and produce cells that undergo differentiation—located at the apices of axes [1].The oldest preserved root apices in which cellular anatomy can be imaged are found in nodules of permineralized fossil soils called coal balls [2], which formed in the Carboniferous coal swamp forests over 300 million years ago [3, 4, 5, 6, 7, 8 and 9]. However, no fossil root apices described to date were actively growing at the time of preservation [3, 4, 5, 6, 7, 8, 9 and 10]. Because the cellular organization of meristems changes when root growth stops, it has been impossible to compare cellular dynamics as stem cells transition to differentiated cells in extinct and extant taxa [11]. We predicted that meristems of actively growing roots would be preserved in coal balls. Here we report the discovery of the first fossilized remains of an actively growing root meristem from permineralized Carboniferous soil with detail of the stem cells and differentiating cells preserved. The cellular organization of the meristem is unique. The position of the Körper-Kappe boundary, discrete root cap, and presence of many anticlinal cell divisions within a broad promeristem distinguish it from all other known root meristems. This discovery is important because it demonstrates that the same general cellular dynamics are conserved between the oldest extinct and extant root meristems. However, its unique cellular organization demonstrates that extant root meristem organization and development represents only a subset of the diversity that has existed since roots first evolved.</p

A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism

A continuum from stem to transit-amplifying to a differentiated cell state is a common theme in multicellular organisms. In the plant root apical meristem (RAM), transit-amplifying cells are organized into two domains: cells from the proliferation domain (PD) are displaced to the transition domain (TD), suggesting that both domains are necessarily coupled. Here, we show that in the Arabidopsis thaliana mto2-2 mutant, in which threonine (Thr) synthesis is affected, the RAM lacks the PD. Through a combination of cell length profile analysis, mathematical modeling and molecular markers, we establish that the PD and TD can be uncoupled. Remarkably, although the RAM of mto2-2 is represented solely by the TD, the known factors of RAM maintenance and auxin signaling are expressed in the mutant. Mathematical modeling predicts that the stem cell niche depends on Thr metabolism and that, when disturbed, the normal continuum of cell states becomes aborted

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

Elucidating molecular links between cell-fate regulatory networks and dynamic patterning modules is a key for understanding development. Auxin is important for plant patterning, particularly in roots, where it establishes positional information for cell-fate decisions. PIN genes encode plasma membrane proteins that serve as auxin efflux transporters; mutations in members of this gene family exhibit smaller roots with altered root meristems and stem-cell patterning. Direct regulators of PIN transcription have remained elusive. Here, we establish that a MADS-box gene (XAANTAL2, XAL2/AGL14) controls auxin transport via PIN transcriptional regulation during Arabidopsis root development; mutations in this gene exhibit altered stem-cell patterning, root meristem size, and root growth. XAL2 is necessary for normal shootward and rootward auxin transport, as well as for maintaining normal auxin distribution within the root. Furthermore, this MADS-domain transcription factor upregulates PIN1 and PIN4 by direct binding to regulatory regions and it is required for PIN4-dependent auxin response. In turn, XAL2 expression is regulated by auxin levels thus establishing a positive feedback loop between auxin levels and PIN regulation that is likely to be important for robust root patterning.This work was supported by grants from CONACYT, México: Red Tematica de Investigacion: ‘Complejidad, Ciencia y Sociedad’ (124909; ERAB; BGP; AGA) and 81542 and 105678 (ERAB), 167705 (AGA), 152649 (MPS), 81433 (BGP), 177739 (SF) and 127957 (JGD), from PAPIIT-UNAM, IN204011-3 (BGP), IN229009-3 (ERAB), IN226510-3 (AGA), IB201212 (MPS), and IN204312 (JGD), from the Spanish Government BFU2012-33746 (SP) and from the National Science Foundation (NSF-IOS) 0820648 (ASM). ERAB acknowledges the support of the Miller Institute for Basic Research in Science, University of California, Berkeley while spending a sabbatical leave in the laboratory of Chelsea Specht at UC-B.Peer reviewe

Longitudinal zonation pattern in Arabidopsis root tip defined by a multiple structural change algorithm

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