@article{9332, abstract = {Lateral root (LR) formation is an example of a plant post-embryonic organogenesis event. LRs are issued from non-dividing cells entering consecutive steps of formative divisions, proliferation and elongation. The chromatin remodeling protein PICKLE (PKL) negatively regulates auxin-mediated LR formation through a mechanism that is not yet known. Here we show that PKL interacts with RETINOBLASTOMA-RELATED 1 (RBR1) to repress the LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16) promoter activity. Since LBD16 function is required for the formative division of LR founder cells, repression mediated by the PKL–RBR1 complex negatively regulates formative division and LR formation. Inhibition of LR formation by PKL–RBR1 is counteracted by auxin, indicating that, in addition to auxin-mediated transcriptional responses, the fine-tuned process of LR formation is also controlled at the chromatin level in an auxin-signaling dependent manner.}, author = {Ötvös, Krisztina and Miskolczi, Pál and Marhavý, Peter and Cruz-Ramírez, Alfredo and Benková, Eva and Robert, Stéphanie and Bakó, László}, issn = {1422-0067}, journal = {International Journal of Molecular Sciences}, number = {8}, publisher = {MDPI}, title = {{Pickle recruits retinoblastoma related 1 to control lateral root formation in arabidopsis}}, doi = {10.3390/ijms22083862}, volume = {22}, year = {2021}, } @article{8336, abstract = {Plant hormone cytokinins are perceived by a subfamily of sensor histidine kinases (HKs), which via a two-component phosphorelay cascade activate transcriptional responses in the nucleus. Subcellular localization of the receptors proposed the endoplasmic reticulum (ER) membrane as a principal cytokinin perception site, while study of cytokinin transport pointed to the plasma membrane (PM)-mediated cytokinin signalling. Here, by detailed monitoring of subcellular localizations of the fluorescently labelled natural cytokinin probe and the receptor ARABIDOPSIS HISTIDINE KINASE 4 (CRE1/AHK4) fused to GFP reporter, we show that pools of the ER-located cytokinin receptors can enter the secretory pathway and reach the PM in cells of the root apical meristem, and the cell plate of dividing meristematic cells. Brefeldin A (BFA) experiments revealed vesicular recycling of the receptor and its accumulation in BFA compartments. We provide a revised view on cytokinin signalling and the possibility of multiple sites of perception at PM and ER.}, author = {Kubiasova, Karolina and Montesinos López, Juan C and Šamajová, Olga and Nisler, Jaroslav and Mik, Václav and Semeradova, Hana and Plíhalová, Lucie and Novák, Ondřej and Marhavý, Peter and Cavallari, Nicola and Zalabák, David and Berka, Karel and Doležal, Karel and Galuszka, Petr and Šamaj, Jozef and Strnad, Miroslav and Benková, Eva and Plíhal, Ondřej and Spíchal, Lukáš}, issn = {20411723}, journal = {Nature Communications}, publisher = {Springer Nature}, title = {{Cytokinin fluoroprobe reveals multiple sites of cytokinin perception at plasma membrane and endoplasmic reticulum}}, doi = {10.1038/s41467-020-17949-0}, volume = {11}, year = {2020}, } @article{6023, abstract = {Multicellular development requires coordinated cell polarization relative to body axes, and translation to oriented cell division 1–3 . In plants, it is unknown how cell polarities are connected to organismal axes and translated to division. Here, we identify Arabidopsis SOSEKI proteins that integrate apical–basal and radial organismal axes to localize to polar cell edges. Localization does not depend on tissue context, requires cell wall integrity and is defined by a transferrable, protein-specific motif. A Domain of Unknown Function in SOSEKI proteins resembles the DIX oligomerization domain in the animal Dishevelled polarity regulator. The DIX-like domain self-interacts and is required for edge localization and for influencing division orientation, together with a second domain that defines the polar membrane domain. Our work shows that SOSEKI proteins locally interpret global polarity cues and can influence cell division orientation. Furthermore, this work reveals that, despite fundamental differences, cell polarity mechanisms in plants and animals converge on a similar protein domain.}, author = {Yoshida, Saiko and Van Der Schuren, Alja and Van Dop, Maritza and Van Galen, Luc and Saiga, Shunsuke and Adibi, Milad and Möller, Barbara and Ten Hove, Colette A. and Marhavy, Peter and Smith, Richard and Friml, Jiří and Weijers, Dolf}, journal = {Nature Plants}, number = {2}, pages = {160--166}, publisher = {Springer Nature}, title = {{A SOSEKI-based coordinate system interprets global polarity cues in arabidopsis}}, doi = {10.1038/s41477-019-0363-6}, volume = {5}, year = {2019}, } @article{6351, abstract = {A process of restorative patterning in plant roots correctly replaces eliminated cells to heal local injuries despite the absence of cell migration, which underpins wound healing in animals. Patterning in plants relies on oriented cell divisions and acquisition of specific cell identities. Plants regularly endure wounds caused by abiotic or biotic environmental stimuli and have developed extraordinary abilities to restore their tissues after injuries. Here, we provide insight into a mechanism of restorative patterning that repairs tissues after wounding. Laser-assisted elimination of different cells in Arabidopsis root combined with live-imaging tracking during vertical growth allowed analysis of the regeneration processes in vivo. Specifically, the cells adjacent to the inner side of the injury re-activated their stem cell transcriptional programs. They accelerated their progression through cell cycle, coordinately changed the cell division orientation, and ultimately acquired de novo the correct cell fates to replace missing cells. These observations highlight existence of unknown intercellular positional signaling and demonstrate the capability of specified cells to re-acquire stem cell programs as a crucial part of the plant-specific mechanism of wound healing.}, author = {Marhavá, Petra and Hörmayer, Lukas and Yoshida, Saiko and Marhavy, Peter and Benková, Eva and Friml, Jiří}, issn = {10974172}, journal = {Cell}, number = {4}, pages = {957--969.e13}, publisher = {Elsevier}, title = {{Re-activation of stem cell pathways for pattern restoration in plant wound healing}}, doi = {10.1016/j.cell.2019.04.015}, volume = {177}, year = {2019}, } @article{1492, abstract = {To sustain a lifelong ability to initiate organs, plants retain pools of undifferentiated cells with a preserved prolif eration capacity. The root pericycle represents a unique tissue with conditional meristematic activity, and its tight control determines initiation of lateral organs. Here we show that the meristematic activity of the pericycle is constrained by the interaction with the adjacent endodermis. Release of these restraints by elimination of endo dermal cells by single-cell ablation triggers the pericycle to re-enter the cell cycle. We found that endodermis removal substitutes for the phytohormone auxin-dependent initiation of the pericycle meristematic activity. However, auxin is indispensable to steer the cell division plane orientation of new organ-defining divisions. We propose a dual, spatiotemporally distinct role for auxin during lateral root initiation. In the endodermis, auxin releases constraints arising from cell-to-cell interactions that compromise the pericycle meristematic activity, whereas, in the pericycle, auxin defines the orientation of the cell division plane to initiate lateral roots.}, author = {Marhavy, Peter and Montesinos López, Juan C and Abuzeineh, Anas and Van Damme, Daniël and Vermeer, Joop and Duclercq, Jérôme and Rakusova, Hana and Marhavá, Petra and Friml, Jirí and Geldner, Niko and Benková, Eva}, journal = {Genes and Development}, number = {4}, pages = {471 -- 483}, publisher = {Cold Spring Harbor Laboratory Press}, title = {{Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation}}, doi = {10.1101/gad.276964.115}, volume = {30}, year = {2016}, } @article{832, abstract = {Plants maintain capacity to form new organs such as leaves, flowers, lateral shoots and roots throughout their postembryonic lifetime. Lateral roots (LRs) originate from a few pericycle cells that acquire attributes of founder cells (FCs), undergo series of anticlinal divisions, and give rise to a few short initial cells. After initiation, coordinated cell division and differentiation occur, giving rise to lateral root primordia (LRP). Primordia continue to grow, emerge through the cortex and epidermal layers of the primary root, and finally a new apical meristem is established taking over the responsibility for growth of mature lateral roots [for detailed description of the individual stages of lateral root organogenesis see Malamy and Benfey (1997)]. To examine this highly dynamic developmental process and to investigate a role of various hormonal, genetic and environmental factors in the regulation of lateral root organogenesis, the real time imaging based analyses represent extremely powerful tools (Laskowski et al., 2008; De Smet et al., 2012; Marhavy et al., 2013 and 2014). Herein, we describe a protocol for real time lateral root primordia (LRP) analysis, which enables the monitoring of an onset of the specific gene expression and subcellular protein localization during primordia organogenesis, as well as the evaluation of the impact of genetic and environmental perturbations on LRP organogenesis.}, author = {Peter Marhavy and Eva Benková}, journal = {Bio-protocol}, number = {8}, publisher = {Bio-protocol LLC}, title = {{Real time analysis of lateral root organogenesis in arabidopsis}}, doi = {10.21769/BioProtoc.1446}, volume = {5}, year = {2015}, } @article{1640, abstract = {Auxin and cytokinin are key endogenous regulators of plant development. Although cytokinin-mediated modulation of auxin distribution is a developmentally crucial hormonal interaction, its molecular basis is largely unknown. Here we show a direct regulatory link between cytokinin signalling and the auxin transport machinery uncovering a mechanistic framework for cytokinin-auxin cross-talk. We show that the CYTOKININ RESPONSE FACTORS (CRFs), transcription factors downstream of cytokinin perception, transcriptionally control genes encoding PIN-FORMED (PIN) auxin transporters at a specific PIN CYTOKININ RESPONSE ELEMENT (PCRE) domain. Removal of this cis-regulatory element effectively uncouples PIN transcription from the CRF-mediated cytokinin regulation and attenuates plant cytokinin sensitivity. We propose that CRFs represent a missing cross-talk component that fine-tunes auxin transport capacity downstream of cytokinin signalling to control plant development.}, author = {Šimášková, Mária and O'Brien, José and Khan-Djamei, Mamoona and Van Noorden, Giel and Ötvös, Krisztina and Vieten, Anne and De Clercq, Inge and Van Haperen, Johanna and Cuesta, Candela and Hoyerová, Klára and Vanneste, Steffen and Marhavy, Peter and Wabnik, Krzysztof T and Van Breusegem, Frank and Nowack, Moritz and Murphy, Angus and Friml, Jiřĺ and Weijers, Dolf and Beeckman, Tom and Benková, Eva}, journal = {Nature Communications}, publisher = {Nature Publishing Group}, title = {{Cytokinin response factors regulate PIN-FORMED auxin transporters}}, doi = {10.1038/ncomms9717}, volume = {6}, year = {2015}, } @article{1574, abstract = {Multiple plant developmental processes, such as lateral root development, depend on auxin distribution patterns that are in part generated by the PIN-formed family of auxin-efflux transporters. Here we propose that AUXIN RESPONSE FACTOR7 (ARF7) and the ARF7-regulated FOUR LIPS/MYB124 (FLP) transcription factors jointly form a coherent feed-forward motif that mediates the auxin-responsive PIN3 transcription in planta to steer the early steps of lateral root formation. This regulatory mechanism might endow the PIN3 circuitry with a temporal 'memory' of auxin stimuli, potentially maintaining and enhancing the robustness of the auxin flux directionality during lateral root development. The cooperative action between canonical auxin signalling and other transcription factors might constitute a general mechanism by which transcriptional auxin-sensitivity can be regulated at a tissue-specific level.}, author = {Chen, Qian and Liu, Yang and Maere, Steven and Lee, Eunkyoung and Van Isterdael, Gert and Xie, Zidian and Xuan, Wei and Lucas, Jessica and Vassileva, Valya and Kitakura, Saeko and Marhavy, Peter and Wabnik, Krzysztof T and Geldner, Niko and Benková, Eva and Le, Jie and Fukaki, Hidehiro and Grotewold, Erich and Li, Chuanyou and Friml, Jirí and Sack, Fred and Beeckman, Tom and Vanneste, Steffen}, journal = {Nature Communications}, publisher = {Nature Publishing Group}, title = {{A coherent transcriptional feed-forward motif model for mediating auxin-sensitive PIN3 expression during lateral root development}}, doi = {10.1038/ncomms9821}, volume = {6}, year = {2015}, } @article{1934, abstract = {The plant hormones auxin and cytokinin mutually coordinate their activities to control various aspects of development [1-9], and their crosstalk occurs at multiple levels [10, 11]. Cytokinin-mediated modulation of auxin transport provides an efficient means to regulate auxin distribution in plant organs. Here, we demonstrate that cytokinin does not merely control the overall auxin flow capacity, but might also act as a polarizing cue and control the auxin stream directionality during plant organogenesis. Cytokinin enhances the PIN-FORMED1 (PIN1) auxin transporter depletion at specific polar domains, thus rearranging the cellular PIN polarities and directly regulating the auxin flow direction. This selective cytokinin sensitivity correlates with the PIN protein phosphorylation degree. PIN1 phosphomimicking mutations, as well as enhanced phosphorylation in plants with modulated activities of PIN-specific kinases and phosphatases, desensitize PIN1 to cytokinin. Our results reveal conceptually novel, cytokinin-driven polarization mechanism that operates in developmental processes involving rapid auxin stream redirection, such as lateral root organogenesis, in which a gradual PIN polarity switch defines the growth axis of the newly formed organ.}, author = {Marhavy, Peter and Duclercq, Jérôme and Weller, Benjamin and Feraru, Elena and Bielach, Agnieszka and Offringa, Remko and Friml, Jirí and Schwechheimer, Claus and Murphy, Angus and Benková, Eva}, journal = {Current Biology}, number = {9}, pages = {1031 -- 1037}, publisher = {Cell Press}, title = {{Cytokinin controls polarity of PIN1-dependent Auxin transport during lateral root organogenesis}}, doi = {10.1016/j.cub.2014.04.002}, volume = {24}, year = {2014}, } @article{2844, abstract = {As soon as a seed germinates, plant growth relates to gravity to ensure that the root penetrates the soil and the shoot expands aerially. Whereas mechanisms of positive and negative orthogravitropism of primary roots and shoots are relatively well understood [1-3], lateral organs often show more complex growth behavior [4]. Lateral roots (LRs) seemingly suppress positive gravitropic growth and show a defined gravitropic set-point angle (GSA) that allows radial expansion of the root system (plagiotropism) [3, 4]. Despite its eminent importance for root architecture, it so far remains completely unknown how lateral organs partially suppress positive orthogravitropism. Here we show that the phytohormone auxin steers GSA formation and limits positive orthogravitropism in LR. Low and high auxin levels/signaling lead to radial or axial root systems, respectively. At a cellular level, it is the auxin transport-dependent regulation of asymmetric growth in the elongation zone that determines GSA. Our data suggest that strong repression of PIN4/PIN7 and transient PIN3 expression limit auxin redistribution in young LR columella cells. We conclude that PIN activity, by temporally limiting the asymmetric auxin fluxes in the tip of LRs, induces transient, differential growth responses in the elongation zone and, consequently, controls root architecture.}, author = {Rosquete, Michel and Von Wangenheim, Daniel and Marhavy, Peter and Barbez, Elke and Stelzer, Ernst and Benková, Eva and Maizel, Alexis and Kleine Vehn, Jürgen}, journal = {Current Biology}, number = {9}, pages = {817 -- 822}, publisher = {Cell Press}, title = {{An auxin transport mechanism restricts positive orthogravitropism in lateral roots}}, doi = {10.1016/j.cub.2013.03.064}, volume = {23}, year = {2013}, } @article{2880, abstract = {Lateral root (LR) formation is initiated when pericycle cells accumulate auxin, thereby acquiring founder cell (FC) status and triggering asymmetric cell divisions, giving rise to a new primordium. How this auxin maximum in pericycle cells builds up and remains focused is not understood. We report that the endodermis plays an active role in the regulation of auxin accumulation and is instructive for FCs to progress during the LR initiation (LRI) phase. We describe the functional importance of a PIN3 (PIN-formed) auxin efflux carrier-dependent hormone reflux pathway between overlaying endodermal and pericycle FCs. Disrupting this reflux pathway causes dramatic defects in the progress of FCs towards the next initiation phase. Our data identify an unexpected regulatory function for the endodermis in LRI as part of the fine-tuning mechanism that appears to act as a check point in LR organogenesis after FCs are specified.}, author = {Marhavy, Peter and Vanstraelen, Marleen and De Rybel, Bert and Zhaojun, Ding and Bennett, Malcolm and Beeckman, Tom and Benková, Eva}, journal = {EMBO Journal}, number = {1}, pages = {149 -- 158}, publisher = {Wiley-Blackwell}, title = {{Auxin reflux between the endodermis and pericycle promotes lateral root initiation}}, doi = {10.1038/emboj.2012.303}, volume = {32}, year = {2013}, } @article{2875, abstract = {Phytohormones are important plant growth regulators that control many developmental processes, such as cell division, cell differentiation, organogenesis and morphogenesis. They regulate a multitude of apparently unrelated physiological processes, often with overlapping roles, and they mutually modulate their effects. These features imply important synergistic and antagonistic interactions between the various plant hormones. Auxin and cytokinin are central hormones involved in the regulation of plant growth and development, including processes determining root architecture, such as root pole establishment during early embryogenesis, root meristem maintenance and lateral root organogenesis. Thus, to control root development both pathways put special demands on the mechanisms that balance their activities and mediate their interactions. Here, we summarize recent knowledge on the role of auxin and cytokinin in the regulation of root architecture with special focus on lateral root organogenesis, discuss the latest findings on the molecular mechanisms of their interactions, and present forward genetic screen as a tool to identify novel molecular components of the auxin and cytokinin crosstalk.}, author = {Bielach, Agnieszka and Duclercq, Jérôme and Peter Marhavy and Eva Benková}, journal = {Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences}, number = {1595}, pages = {1469 -- 1478}, publisher = {Royal Society, The}, title = {{Genetic approach towards the identification of auxin - cytokinin crosstalk components involved in root development}}, doi = {10.1098/rstb.2011.0233}, volume = {367}, year = {2012}, } @article{829, abstract = {The architecture of a plant's root system, established postembryonically, results from both coordinated root growth and lateral root branching. The plant hormones auxin and cytokinin are central endogenous signaling molecules that regulate lateral root organogenesis positively and negatively, respectively. Tight control and mutual balance of their antagonistic activities are particularly important during the early phases of lateral root organogenesis to ensure continuous lateral root initiation (LRI) and proper development of lateral root primordia (LRP). Here, we show that the early phases of lateral root organogenesis, including priming and initiation, take place in root zones with a repressed cytokinin response. Accordingly, ectopic overproduction of cytokinin in the root basal meristem most efficiently inhibits LRI. Enhanced cytokinin responses in pericycle cells between existing LRP might restrict LRI near existing LRP and, when compromised, ectopic LRI occurs. Furthermore, our results demonstrate that young LRP are more sensitive to perturbations in the cytokinin activity than are developmentally more advanced primordia. We hypothesize that the effect of cytokinin on the development of primordia possibly depends on the robustness and stability of the auxin gradient.}, author = {Bielach, Agnieszka and Podlesakova, Katerina and Peter Marhavy and Duclercq, Jérôme and Candela Cuesta and Muller, Bruno and Grunewald, Wim and Tarkowski, Petr and Eva Benková}, journal = {The Plant Cell}, number = {10}, pages = {3967 -- 3981}, publisher = {American Society of Plant Biologists}, title = {{Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin}}, doi = {10.1105/tpc.112.103044}, volume = {24}, year = {2012}, } @article{3097, abstract = {Cytokinin is an important regulator of plant growth and development. In Arabidopsis thaliana, the two-component phosphorelay mediated through a family of histidine kinases and response regulators is recognized as the principal cytokinin signal transduction mechanism activating the complex transcriptional response to control various developmental processes. Here, we identified an alternative mode of cytokinin action that uses endocytic trafficking as a means to direct plant organogenesis. This activity occurs downstream of known cytokinin receptors but through a branch of the cytokinin signaling pathway that does not involve transcriptional regulation. We show that cytokinin regulates endocytic recycling of the auxin efflux carrier PINFORMED1 (PIN1) by redirecting it for lytic degradation in vacuoles. Stimulation of the lytic PIN1 degradation is not a default effect for general downregulation of proteins from plasma membranes, but a specific mechanism to rapidly modulate the auxin distribution in cytokinin-mediated developmental processes.}, author = {Peter Marhavy and Bielach, Agnieszka and Abas, Lindy and Abuzeineh, Anas and Duclercq, Jérôme and Tanaka, Hirokazu and Pařezová, Markéta and Petrášek, Jan and Jirí Friml and Kleine-Vehn, Jürgen and Eva Benková}, journal = {Developmental Cell}, number = {4}, pages = {796 -- 804}, publisher = {Cell Press}, title = {{Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis}}, doi = {10.1016/j.devcel.2011.08.014}, volume = {21}, year = {2011}, } @article{3065, abstract = {The apical hook of dark-grown Arabidopsis seedlings is a simple structure that develops soon after germination to protect the meristem tissues during emergence through the soil and that opens upon exposure to light. Differential growth at the apical hook proceeds in three sequential steps that are regulated by multiple hormones, principally auxin and ethylene. We show that the progress of the apical hook through these developmental phases depends on the dynamic, asymmetric distribution of auxin, which is regulated by auxin efflux carriers of the PIN family. Several PIN proteins exhibited specific, partially overlapping spatial and temporal expression patterns, and their subcellular localization suggested auxin fluxes during hook development. Genetic manipulation of individual PIN activities interfered with different stages of hook development, implying that specific combinations of PIN genes are required for progress of the apical hook through the developmental phases. Furthermore, ethylene might modulate apical hook development by prolonging the formation phase and strongly suppressing the maintenance phase. This ethylene effect is in part mediated by regulation of PIN-dependent auxin efflux and auxin signaling.}, author = {Žádníková, Petra and Petrášek, Jan and Peter Marhavy and Raz, Vered and Vandenbussche, Filip and Ding, Zhaojun and Schwarzerová, Kateřina and Morita, Miyo T and Tasaka, Masao and Hejátko, Jan and Van Der Straeten, Dominique and Jirí Friml and Eva Benková}, journal = {Development}, number = {4}, pages = {607 -- 617}, publisher = {Company of Biologists}, title = {{Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana}}, doi = {10.1242/dev.041277}, volume = {137}, year = {2010}, }