@article{6897,
  abstract     = {The apical hook is a transiently formed structure that plays a protective role when the germinating seedling penetrates through the soil towards the surface. Crucial for proper bending is the local auxin maxima, which defines the concave (inner) side of the hook curvature. As no sign of asymmetric auxin distribution has been reported in embryonic hypocotyls prior to hook formation, the question of how auxin asymmetry is established in the early phases of seedling germination remains largely unanswered. Here, we analyzed the auxin distribution and expression of PIN auxin efflux carriers from early phases of germination, and show that bending of the root in response to gravity is the crucial initial cue that governs the hypocotyl bending required for apical hook formation. Importantly, polar auxin transport machinery is established gradually after germination starts as a result of tight root-hypocotyl interaction and a proper balance between abscisic acid and gibberellins.},
  author       = {Zhu, Qiang and Gallemi, Marçal and Pospíšil, Jiří and Žádníková, Petra and Strnad, Miroslav and Benková, Eva},
  issn         = {14779129},
  journal      = {Development},
  number       = {17},
  publisher    = {The Company of Biologists},
  title        = {{Root gravity response module guides differential growth determining both root bending and apical hook formation in Arabidopsis}},
  doi          = {10.1242/dev.175919},
  volume       = {146},
  year         = {2019},
}

@article{1153,
  abstract     = {Differential cell growth enables flexible organ bending in the presence of environmental signals such as light or gravity. A prominent example of the developmental processes based on differential cell growth is the formation of the apical hook that protects the fragile shoot apical meristem when it breaks through the soil during germination. Here, we combined in silico and in vivo approaches to identify a minimal mechanism producing auxin gradient-guided differential growth during the establishment of the apical hook in the model plant Arabidopsis thaliana. Computer simulation models based on experimental data demonstrate that asymmetric expression of the PIN-FORMED auxin efflux carrier at the concave (inner) versus convex (outer) side of the hook suffices to establish an auxin maximum in the epidermis at the concave side of the apical hook. Furthermore, we propose a mechanism that translates this maximum into differential growth, and thus curvature, of the apical hook. Through a combination of experimental and in silico computational approaches, we have identified the individual contributions of differential cell elongation and proliferation to defining the apical hook and reveal the role of auxin-ethylene crosstalk in balancing these two processes. © 2016 American Society of Plant Biologists. All rights reserved.},
  author       = {Žádníková, Petra and Wabnik, Krzysztof T and Abuzeineh, Anas and Gallemí, Marçal and Van Der Straeten, Dominique and Smith, Richard and Inze, Dirk and Friml, Jirí and Prusinkiewicz, Przemysław and Benková, Eva},
  journal      = {Plant Cell},
  number       = {10},
  pages        = {2464 -- 2477},
  publisher    = {American Society of Plant Biologists},
  title        = {{A model of differential growth guided apical hook formation in plants}},
  doi          = {10.1105/tpc.15.00569},
  volume       = {28},
  year         = {2016},
}

@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{1593,
  abstract     = {Plants are sessile organisms that are permanently restricted to their site of germination. To compensate for their lack of mobility, plants evolved unique mechanisms enabling them to rapidly react to ever changing environmental conditions and flexibly adapt their postembryonic developmental program. A prominent demonstration of this developmental plasticity is their ability to bend organs in order to reach the position most optimal for growth and utilization of light, nutrients, and other resources. Shortly after germination, dicotyledonous seedlings form a bended structure, the so-called apical hook, to protect the delicate shoot meristem and cotyledons from damage when penetrating through the soil. Upon perception of a light stimulus, the apical hook rapidly opens and the photomorphogenic developmental program is activated. After germination, plant organs are able to align their growth with the light source and adopt the most favorable orientation through bending, in a process named phototropism. On the other hand, when roots and shoots are diverted from their upright orientation, they immediately detect a change in the gravity vector and bend to maintain a vertical growth direction. Noteworthy, despite the diversity of external stimuli perceived by different plant organs, all plant tropic movements share a common mechanistic basis: differential cell growth. In our review, we will discuss the molecular principles underlying various tropic responses with the focus on mechanisms mediating the perception of external signals, transduction cascades and downstream responses that regulate differential cell growth and consequently, organ bending. In particular, we highlight common and specific features of regulatory pathways in control of the bending of organs and a role for the plant hormone auxin as a key regulatory component.},
  author       = {Žádníková, Petra and Smet, Dajo and Zhu, Qiang and Van Der Straeten, Dominique and Benková, Eva},
  journal      = {Frontiers in Plant Science},
  number       = {4},
  publisher    = {Frontiers Research Foundation},
  title        = {{Strategies of seedlings to overcome their sessile nature: Auxin in mobility control}},
  doi          = {10.3389/fpls.2015.00218},
  volume       = {6},
  year         = {2015},
}

@article{1922,
  abstract     = {Germination of Arabidopsis seeds in darkness induces apical hook development, based on a tightly regulated differential growth coordinated by a multiple hormone cross-talk. Here, we endeavoured to clarify the function of brassinosteroids (BRs) and cross-talk with ethylene in hook development. An automated infrared imaging system was developed to study the kinetics of hook development in etiolated Arabidopsis seedlings. To ascertain the photomorphogenic control of hook opening, the system was equipped with an automatic light dimmer. We demonstrate that ethylene and BRs are indispensable for hook formation and maintenance. Ethylene regulation of hook formation functions partly through BRs, with BR feedback inhibition of ethylene action. Conversely, BR-mediated extension of hook maintenance functions partly through ethylene. Furthermore, we revealed that a short light pulse is sufficient to induce rapid hook opening. Our dynamic infrared imaging system allows high-resolution, kinetic imaging of up to 112 seedlings in a single experimental run. At this high throughput, it is ideally suited to rapidly gain insight in pathway networks. We demonstrate that BRs and ethylene cooperatively regulate apical hook development in a phase-dependent manner. Furthermore, we show that light is a predominant regulator of hook opening, inhibiting ethylene- and BR-mediated postponement of hook opening.},
  author       = {Smet, Dajo and Žádníková, Petra and Vandenbussche, Filip and Benková, Eva and Van Der Straeten, Dominique},
  journal      = {New Phytologist},
  number       = {4},
  pages        = {1398 -- 1411},
  publisher    = {Wiley-Blackwell},
  title        = {{Dynamic infrared imaging analysis of apical hook development in Arabidopsis: The case of brassinosteroids}},
  doi          = {10.1111/nph.12751},
  volume       = {202},
  year         = {2014},
}

@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{2472,
  abstract     = {Plant-specific PIN-formed (PIN) efflux transporters for the plant hormone auxin are required for tissue-specific directional auxin transport and cellular auxin homeostasis. The Arabidopsis PIN protein family has been shown to play important roles in developmental processes such as embryogenesis, organogenesis, vascular tissue differentiation, root meristem patterning and tropic growth. Here we analyzed roles of the less characterised Arabidopsis PIN6 auxin transporter. PIN6 is auxin-inducible and is expressed during multiple auxin-regulated developmental processes. Loss of pin6 function interfered with primary root growth and lateral root development. Misexpression of PIN6 affected auxin transport and interfered with auxin homeostasis in other growth processes such as shoot apical dominance, lateral root primordia development, adventitious root formation, root hair outgrowth and root waving. These changes in auxin-regulated growth correlated with a reduction in total auxin transport as well as with an altered activity of DR5-GUS auxin response reporter. Overall, the data indicate that PIN6 regulates auxin homeostasis during plant development.},
  author       = {Cazzonelli, Christopher and Vanstraelen, Marleen and Simon, Sibu and Yin, Kuide and Carron Arthur, Ashley and Nisar, Nazia and Tarle, Gauri and Cuttriss, Abby and Searle, Iain and Benková, Eva and Mathesius, Ulrike and Masle, Josette and Friml, Jirí and Pogson, Barry},
  journal      = {PLoS One},
  number       = {7},
  publisher    = {Public Library of Science},
  title        = {{Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development}},
  doi          = {10.1371/journal.pone.0070069},
  volume       = {8},
  year         = {2013},
}

@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{827,
  abstract     = {As sessile organisms, plants have to be able to adapt to a continuously changing environment. Plants that perceive some of these changes as stress signals activate signaling pathways to modulate their development and to enable them to survive. The complex responses to environmental cues are to a large extent mediated by plant hormones that together orchestrate the final plant response. The phytohormone cytokinin is involved in many plant developmental processes. Recently, it has been established that cytokinin plays an important role in stress responses, but does not act alone. Indeed, the hormonal control of plant development and stress adaptation is the outcome of a complex network of multiple synergistic and antagonistic interactions between various hormones. Here, we review the recent findings on the cytokinin function as part of this hormonal network. We focus on the importance of the crosstalk between cytokinin and other hormones, such as abscisic acid, jasmonate, salicylic acid, ethylene, and auxin in the modulation of plant development and stress adaptation. Finally, the impact of the current research in the biotechnological industry will be discussed.},
  author       = {O'Brien, José and Benková, Eva},
  journal      = {Frontiers in Plant Science},
  publisher    = {Frontiers Research Foundation},
  title        = {{Cytokinin cross talking during biotic and abiotic stress responses}},
  doi          = {10.3389/fpls.2013.00451},
  volume       = {4},
  year         = {2013},
}

@article{828,
  abstract     = {The plant root system is essential for providing anchorage to the soil, supplying minerals and water, and synthesizing metabolites. It is a dynamic organ modulated by external cues such as environmental signals, water and nutrients availability, salinity and others. Lateral roots (LRs) are initiated from the primary root post-embryonically, after which they progress through discrete developmental stages which can be independently controlled, providing a high level of plasticity during root system formation. Within this review, main contributions are presented, from the classical forward genetic screens to the more recent high-throughput approaches, combined with computer model predictions, dissecting how LRs and thereby root system architecture is established and developed.},
  author       = {Cuesta, Candela and Wabnik, Krzysztof T and Benková, Eva},
  journal      = {Frontiers in Plant Science},
  publisher    = {Frontiers Research Foundation},
  title        = {{Systems approaches to study root architecture dynamics}},
  doi          = {10.3389/fpls.2013.00537},
  volume       = {4},
  year         = {2013},
}

