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- W3004183610 abstract "The development of lateral roots requires multiple mechanisms that act together for accurate spatiotemporal emergence of the new organ. A new paper shows how cell death in overlying endodermis cells contributes to the formation of new lateral root primordia. The development of lateral roots requires multiple mechanisms that act together for accurate spatiotemporal emergence of the new organ. A new paper shows how cell death in overlying endodermis cells contributes to the formation of new lateral root primordia. Plants cannot change their spatial location and therefore rely heavily on post-embryonic organ formation to cope with changing environmental conditions. This is analogous to adaptive behavior of animals in response to their surroundings. For de novo post-embryonic morphogenesis of organs such as leaves, branches and lateral roots, plants retain groups of undifferentiated cells known as meristems that allow them to constantly produce new cells and organs during their entire life span. In the above-ground parts of the plant, lateral organs initiate as primordia on the flanks of the meristem, and eventually give rise to new branches, leaves, flowers and inflorescences. However, lateral roots rarely form near the root meristem [1Hetherington A.J. Dolan L. The evolution of lycopsid rooting structures: conservatism and disparity.New Phytol. 2016; 215: 538-544Crossref PubMed Scopus (38) Google Scholar], but rather in more proximal regions where most tissues have already undergone differentiation. To allow new lateral root primordia to initiate, a single tissue within the root, the pericycle, maintains cell division capacity, contrary to the surrounded differentiated cells [2Dubrovsky J.G. Doerner P.W. Colón-Carmona A. Rost T.L. Pericycle cell proliferation and lateral root initiation in Arabidopsis.Plant Physiol. 2000; 124: 1648-1657Crossref PubMed Scopus (190) Google Scholar]. When a lateral root is starting to form at a specific location along the main root, a small population of pericycle cells will undergo several rounds of cell divisions that go on to form the lateral root primordium. Because the pericycle is an internal tissue, the lateral root primordium must make its way through the overlying tissue layers to emerge as a new lateral root. In the past two decades, dozens of genes belonging to several pathways have been implicated in lateral root primordia initiation [3Banda J. Bellande K. Wangenheim von D. Goh T. Guyomarc'h S. Laplaze L. Bennett M.J. Lateral root formation in Arabidopsis: A well-ordered LRexit.Trends Plant Sci. 2019; 24: 826-839Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar]. Pathways involving the plant hormone auxin are by far the most studied with respect to lateral root development, sometimes to an extent that masks the importance of other mechanisms in this process. Several genes involved in auxin signaling, biosynthesis and transport have specific effects on the initiation of lateral roots [4Du Y. Scheres B. Lateral root formation and the multiple roles of auxin.J. Exp. Bot. 2017; 69: 155-167Crossref Scopus (179) Google Scholar]. For example, the arf7 arf19 double mutant as well as the gain-of-function slr mutant, both of which are involved in auxin signaling, have no lateral roots [5Okushima Y. Overvoorde P.J. Arima K. Alonso J.M. Chan A. Chang C. Ecker J.R. Hughes B. Lui A. Nguyen D. et al.Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19.Plant Cell. 2005; 17: 444-463Crossref PubMed Scopus (759) Google Scholar]. Many other mechanisms, including regulation of water diffusion by aquaporins [6Reinhardt H. Hachez C. Bienert M.D. Beebo A. Swarup K. Voß U. Bouhidel K. Frigerio L. Schjoerring J.K. Bennett M.J. et al.Tonoplast aquaporins facilitate lateral root emergence.Plant Physiol. 2016; 170: 1640-1654Crossref PubMed Scopus (45) Google Scholar] and ethylene biosynthesis [7Prasad M.E. Schofield A. Lyzenga W. Liu H. Stone S.L. Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis.Plant Physiol. 2010; 153: 1587-1596Crossref PubMed Scopus (72) Google Scholar], have been shown to be required for the formation of lateral root primordia. Taken together, the formation of lateral roots is a complex process that requires the participation of multiple molecular mechanisms. In this issue of Current Biology, Escamez et al. [8Escamez S. Andre D. Sztojka D. Bollhöner B. Hall H. Berthet B. Voß U. Lers A. Maizel A. Andersson M. et al.Cell death in cells overlying lateral root primordia facilitates organ growth in Arabidopsis.Curr. Biol. 2019; 30: 455-464Abstract Full Text Full Text PDF Scopus (18) Google Scholar] show how cell death-related genes contribute to the developmental progression of lateral root primordia. Interestingly, previous publications demonstrated that induction of cell death in the endodermis is sufficient to induce cell division in the underlying pericycle, but it does not result in lateral root primordia initiation [9Marhavý P. Montesinos J.C. Abuzeineh A. Van Damme D. Vermeer J.E.M. Duclercq J. Rakusova H. Novakova P. Friml J. Geldner N. et al.Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation.Genes Dev. 2016; 30: 471-483Crossref PubMed Scopus (57) Google Scholar]. Bonnett has shown that cortical parenchyma cells overlying lateral root primordia in bindweed undergo cell death [10Bonnett H.T. Cortical cell death during lateral root formation.J. Cell Biol. 1969; 40: 144-159Crossref PubMed Scopus (39) Google Scholar], while Vermeer et al. [11Vermeer J.E.M. Wangenheim von D. Barberon M. Lee Y. Stelzer E.H.K. Maizel A. Geldner N. A spatial accommodation by neighboring cells Is required for organ initiation in Arabidopsis.Science. 2014; 343: 174-178Crossref PubMed Scopus (187) Google Scholar] provided evidence that endodermal cells undergo morphological changes during the formation of underlying lateral root primordia, which are required for progression of this process. In the first part of their manuscript, Escamez et al. show that a set of core genes specifically expressed in tissues that undergo developmental cell death and autolysis [12Olvera-Carrillo Y. Van Bel M. Van Hautegem T. Fendrych M. Van Durme M. Huysmans M. Simaskova M. Buscalli P. Rivas S. Coll N.S. et al.A conserved core of PCD indicator genes discriminates developmentally and environmentally induced programmed cell death in plants.Plant Physiol. 2015; 169: 2684-2699PubMed Google Scholar] are also expressed in endodermal cells overlying lateral root primordia. It is interesting to note that the spatiotemporal expression of some of these proteins such as BFN1 is restricted not only to the lateral root primordia position, but also to a time window of less than 14 hours during which the primordia emerge through the endodermis. Additional cell death markers as well as transmission electron microscopic examination allowed the authors to validate this initial observation. Next, the authors showed how mutations in ORE1, a regulator of genes involved in cell death and cell wall remodeling, lead to reduction in the number of emerging lateral roots. This phenotype could be partially rescued by either tissue-specific induction of endodermis cell death using the pro-apoptotic mBAX protein or by laser ablation of endodermis cells overlying lateral root primordia. The current study by Escamez et al. raises several interesting questions regarding the importance of cell death during lateral root development. First, the phenotype of the ore1 mutants is very mild — lateral root primordia do form, but their developmental stage distribution is skewed as compared to wild type. A future study might determine whether the role of ORE1 (and the cell death mechanism) in the endodermis is merely to promote developmental progression of lateral root primordia towards mature lateral roots. Alternatively, the reason for the mild phenotype may be functional redundancy; therefore, one could test whether a double mutant of both ORE1 and its closest homolog ORS1 would result in a more severe phenotype. Interestingly, ORS1 is mainly expressed in epidermis and cortex cell layers [13Li S. Yamada M. Han X. Ohler U. Benfey P.N. High-resolution expression map of the Arabidopsis root Reveals alternative splicing and lincRNA regulation.Dev. Cell. 2016; 39: 508-522Abstract Full Text Full Text PDF PubMed Scopus (155) Google Scholar] with low expression in the endodermis. Previous work on bindweed [10Bonnett H.T. Cortical cell death during lateral root formation.J. Cell Biol. 1969; 40: 144-159Crossref PubMed Scopus (39) Google Scholar] showed that cortex cells, rather than endodermis cells overlying lateral root primordia, undergo cell death. Since the lateral root primordia in Arabidopsis have to penetrate through the cortex and the epidermis (in addition to the endodermis) it is possible that cell death induction is required in these layers as well. It will be interesting to see how future research on lateral root initiation involving cell death mechanisms unfolds and specifically whether other genes, especially homologs of the genes investigated in the current study, participate in this process. Cell Death in Cells Overlying Lateral Root Primordia Facilitates Organ Growth in ArabidopsisEscamez et al.Current BiologyJanuary 16, 2020In BriefEscamez et al. report that a subset of cells overlying newly formed lateral roots within the parent root dies to facilitate early lateral root organ growth. Our findings suggest that, contrary to common belief, cell death can, as in animals, regulate organ growth in plants, which may have implications for our understanding of evolution. Full-Text PDF Open Access" @default.
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- W3004183610 title "Lateral Root Initiation: The Emergence of New Primordia Following Cell Death" @default.
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