Cell-to-Cell Communication during Lateral Root Development

Abstract

Cell-to-cell communication plays an important role in coordinating development and specifying cell fate in all multicellular organisms. In plants, wherein cells are immobilized and trapped within a bodice of cellulosic cell walls, exchange of positional information required for normal organogenesis has recently become the object of a growing area of research. The branching of roots through progressive formation of lateral roots is a major determinant of root systems architecture to assist plants in water uptake, acquisition of nutrients, and anchorage. During the exploration of the soil, a sequential specification of lateral root founder cells occurs in the pericycle, followed by a regular sequence of cell divisions culminating in the growth of a primordia through the overlying tissues. To cope with environmental stresses, the entire process has to be tightly controlled and heavily relies on correct communication between cells that transport and exchange signals from the environment or other tissues in the plant. Over recent decades, plant hormones such as auxin and cytokinin have been studied as important messengers to coordinate lateral root formation. Only recently, an increasing number of studies reported on the potential involvement of cell communication systems for this developmental process (Figure 1). In Arabidopsis, more than 1000 genes encoding putative secreted peptides have been identified supporting the hypothesis that peptide–ligand receptor pairs act in cell-to-cell communication to regulate developmental processes. In recent years, an accumulating number of receptor kinases and signaling peptides has been related to cell-to-cell communication in the root. The GOLVEN/ROOT GROWTH FACTOR/CLAVATA-EMBRYO SURROUNDING REGION RELATED (CLE)-Like (GLV/RGF/CLEL) peptide family, originally described to promote primary root elongation growth, was recently associated with lateral root development. Overexpression of CLEL6 and CLEL7 significantly blocked lateral root formation in Arabidopsis seedlings (Meng et al., 2012Meng L. Buchanan B.B. Feldman L.J. Luan S. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis.Proc. Natl Acad. Sci. U S A. 2012; 109: 1760-1765Crossref PubMed Scopus (122) Google Scholar). Closer inspection of this phenotype showed that lateral root founder cells in these mutants divided both asymmetrically and symmetrically instead of strictly asymmetrically. This deviation from the normal division pattern seemed to be correlated with a reduced ability of the LRP to form a central core of small daughter cells which impaired further development. Overexpression of other members of the same family also resulted in a decreased lateral root number. Furthermore, these genes are expressed during different developmental stages of lateral root formation—a manifestation of their potential role in the progression through certain developmental stages (Meng et al., 2012Meng L. Buchanan B.B. Feldman L.J. Luan S. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis.Proc. Natl Acad. Sci. U S A. 2012; 109: 1760-1765Crossref PubMed Scopus (122) Google Scholar; Fernandez et al., 2013Fernandez A. Drozdzecki A. Hoogewijs K. Nguyen A. Beeckman T. Madder A. Hilson P. Transcriptional and functional classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-like signaling peptides reveals their role in lateral root and hair formation.Plant Physiol. 2013; 161: 954-970Crossref PubMed Scopus (83) Google Scholar). Another peptide of the CLE family, TRACHEARY ELEMENT DIFFERENTION INHIBITOR FACTOR (TDIF), was recently shown to be part of a signaling cascade that controls regulation of ARF and AUX/IAA interaction, independently of auxin perception during lateral root development (Cho et al., 2014Cho H. Ryu H. Rho S. Hill K. Smith S. Audenaert D. Park J. Han S. Beeckman T. Bennett M.J. et al.A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development.Nat. Cell Biol. 2014; 16: 66-76Crossref PubMed Scopus (196) Google Scholar). During emergence, lateral root primordia need to break through the overlaying tissues (endodermal, cortex, and epidermal) to grow out, requiring an active cell separation process. Recent research reports that the INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) and IDA-like (IDL)-dependent signaling regulates cell wall degrading and remodeling genes, and controls pectin degradation and consequently the separation of the tissues overlying the lateral root primordia (Kumpf et al., 2013Kumpf R.P. Shi C.L. Larrieu A. Sto I.M. Butenko M.A. Peret B. Riiser E.S. Bennett M.J. Aalen R.B Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence.Proc. Natl Acad. Sci. U S A. 2013; 110: 5235-5240Crossref PubMed Scopus (159) Google Scholar). C-terminally encoded peptide (CEP) family members have been implicated in various developmental processes including root elongation, lateral root development, and environmental responses (Delay et al., 2013Delay C. Imin N. Djordjevic M.A CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants.J. Exp. Bot. 2013; 64: 5383-5394Crossref PubMed Scopus (104) Google Scholar). In the Arabidopsis root, CEP1 is mainly expressed in the lateral root primordia. Overexpression of several CEP genes or treatment with synthetic peptides slowed down primary root growth and reduced lateral root formation, arguing for an inhibitory function during root development (Ohyama et al., 2008Ohyama K. Ogawa M. Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis.Plant J. 2008; 55: 152-160Crossref PubMed Scopus (192) Google Scholar). Arabidopsis CRINKLY4 (ACR4), the first receptor-like kinase that was reported to play a crucial role in lateral root formation, is transcriptionally induced in the small daughter cells resulting from the first asymmetric cell division of the lateral root founder cells. Through knockout studies, it became clear that ACR4-dependent signaling is required to limit the number of asymmetric cell division cycles, with acr4 mutants frequently showing extended primordial stages. Being localized centrally and restraining cell proliferation in neighboring cells, the ACR4-based cell communication is proposed to be part of a lateral inhibition mechanism restricting the number of founder cell divisions in the pericycle (De Smet et al., 2008De Smet I. Vassileva V. De Rybel B. Levesque M.P. Grunewald W. Van Damme D. Van Noorden G. Naudts M. Van Isterdael G. De Clercq R. et al.Receptor-like kinase ACR4 restricts formative cell divisions in the s root.Science. 2008; 322: 594-597Crossref PubMed Scopus (285) Google Scholar). Likewise, in the root tip, ACR4 restrains columella stem cell divisions (De Smet et al., 2008De Smet I. Vassileva V. De Rybel B. Levesque M.P. Grunewald W. Van Damme D. Van Noorden G. Naudts M. Van Isterdael G. De Clercq R. et al.Receptor-like kinase ACR4 restricts formative cell divisions in the s root.Science. 2008; 322: 594-597Crossref PubMed Scopus (285) Google Scholar), is activated by the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION40 (CLE40), and was recently shown to form heterodimers (besides its homodimerization) with CLV1, a well-known receptor-like kinase controlling stem cell divisions in the shoot apical meristem (Stahl et al., 2013Stahl Y. Grabowski S. Bleckmann A. Kuhnemuth R. Weidtkamp-Peters S. Pinto K.G. Kirschner G.K. Schmid J.B. Wink R.H. Hulsewede A. et al.Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase Complexes.Curr. Biol. 2013; 23: 362-371Abstract Full Text Full Text PDF PubMed Scopus (263) Google Scholar). Interestingly, ACR4 and CLV1 co-localize at the plasma membrane and at the plasmodesmata (PDs). PDs are plant-specific structures that form plasma membrane-lined pores traversing the cell walls of neighboring cells and represent an important means of cell-to-cell communication (Figure 1). Transmission of messages, including transcription factors in the form of non-cell-autonomous proteins, may occur through PDs. Transport through PDs is regulated by callose turnover with callose props at the border of the PDs regulating the passage. It is not clear to what extent and how ACR4-dependent signaling at the PDs contributes to lateral root formation but PD-localized proteins involved in callose degradation (plasmodesmal-localized β-1,3-glucanase1 (PdBG1) and PdBG2) were identified and related to the formation of lateral roots. The knockout mutants pdbg1 and pdbg2 displayed an increase in lateral root density while the overexpression plants showed a significant decrease. Closer examination of loss-of-function mutant roots showed that the primordia were frequently formed adjacent to each other and resulted in the formation of fused lateral roots. PdBG1 and PdBG2 are localized at PDs of early stages LRP and in provascular and vascular tissue of basal meristem. In the pdbg1,2 double mutant, excessive callose deposition obstructs PDs thereby blocking symplastic intercellular transport that is required for a correct spatial distribution of lateral roots along the primary root (Benitez-Alfonso et al., 2013Benitez-Alfonso Y. Faulkner C. Pendle A. Miyashima S. Helariutta Y. Maule A. Symplastic intercellular connectivity regulates lateral root patterning.Dev. Cell. 2013; 26: 136-147Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar). Besides cell-to-cell communication through ligand receptor modules at the plasma–membrane and PDs traversing the cell wall, a third research area related to cell-to-cell communication has also reached the field of root development. In plants, phloem is the living tissue that carries organic nutrients and mobile signals, including proteins, small RNAs, and full-length transcripts, from mature leaves to developing sink tissues (Figure 1). Recent studies highlighted the importance of phloem-derived signaling in the root. A new stem-grafting system with Arabidopsis as donor stock and Nicotiana benthamiana as the recipient scion was developed to detect the phloem transport of Aux/IAA transcripts. In Arabidopsis, IAA18 and IAA28 are expressed in the vascular tissue of mature leaves; the mRNA extracted from hetero-grafted N. benthamiana confirmed the transportation from the leaves to the root tips through the phloem. After delivery to primary and lateral roots, these transcripts move from cell to cell via plasmodesmata and are supposed to negatively regulate root branching (Notaguchi et al., 2012Notaguchi M. Wolf S. Lucas W.J Phloem-mobile Aux/IAA transcripts target to the root tip and modify root architecture.Journal of Integrative Plant Biology. 2012; 54: 760-772Crossref PubMed Scopus (94) Google Scholar). In potato, StBEL5 transcripts are transported from leaves through the phloem to stolon tips and enhance tuber formation. They also move into both primary and lateral roots, locally influence auxin levels and modulating root growth (Hannapel et al., 2013Hannapel D.J. Sharma P. Lin T. Phloem-mobile messenger RNAs and root development.Frontiers in Plant Science. 2013; 4: 257PubMed Google Scholar). In Arabidopsis, lateral roots are produced at the xylem poles but evidence for the existence of a phloem-derived cell-to-cell communication system that interferes with lateral root development came from a study of phloem-localized GLUTAMATE RECEPTOR-LIKE (GLR) proteins (Vincill et al., 2013Vincill E.D. Clarin A.E. Molenda J.N. Spalding E.P Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis.Plant Cell. 2013; 25: 1304-1313Crossref PubMed Scopus (90) Google Scholar). GLATERAL ROOT3.2 (GLR3.2) and GLATERAL ROOT3.4 (GLR3.4) represent heteromeric, amino acid-gated Ca2+ channels. Their loss-of-function mutants overproduced lateral root primordia in ectopic positions, but without changing the number of emerged lateral roots. It is therefore proposed that these channels play a role as negative regulators of lateral root initiation, restricting LRP numbers by a signaling process originating from the phloem. Over the past few months, independent studies have highlighted the importance of various types of cell-to-cell communication for the process of root branching. Here, we have summarized these novel findings and conclude that a variety of mobile factors (hormones, peptides, miRNAs, transcription factors) can be transported and perceived in different tissues and cell types to control the initiation and patterning of lateral roots along the main root. We hope this short review will inspire further research in this growing area.