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Authors: Wenguang Wang, Hengbin Gao, Yan Liang, Jiayang Li and Yonghong Wang.
Molecular Plant (2022)
Abstract: "Crop plant architecture is an important agronomic trait that contributes greatly to crop yield. Tiller angle is one of the most critical components that determine crop plant architecture, which in turn substantially affects grain yield mainly owing to its large influence on plant density. Gravity is a fundamental physical force that acts on all organisms on earth. Plant organs sense gravity to control their growth orientation, including tiller angle in rice (Oryza sativa). This review summarizes recent research advances made using rice tiller angle as a research model, providing insights into domestication of rice tiller angle, genetic regulation of rice tiller angle, and shoot gravitropism. Finally, we propose that current discoveries in rice can shed light on shoot gravitropism and improvement of plant tiller/branch angle in other species, thereby contributing to agricultural production in the future."
Authors: Lanxin Li, Michelle Gallei and Jiří Friml.
Trends in Plant Science (2022)
Highlights: The Acid Growth Theory applies to both shoots and roots but the mechanisms of auxin-triggered apoplastic pH regulations are different. Auxin activates plasma membrane (PM) H+-ATPases both in shoots and roots, contributing to shoot growth promotion while counteracting root growth inhibition. Cell surface TMK1 signaling directly activates PM H+-ATPases for apoplast acidification in both shoots and roots. Intracellular TIR1/AFB auxin signaling, besides transcriptional regulation, has a non-transcriptional branch mediating apoplast alkalinization in roots. Auxin-induced rapid apoplast alkalinization in roots occurs not through PM H+-ATPase regulation, but by an unidentified mechanism of H+ influx.
Abstract: "The phytohormone auxin is the major growth regulator governing tropic responses including gravitropism. Auxin build-up at the lower side of stimulated shoots promotes cell expansion, whereas in roots it inhibits growth, leading to upward shoot bending and downward root bending, respectively. Yet it remains an enigma how the same signal can trigger such opposite cellular responses. In this review, we discuss several recent unexpected insights into the mechanisms underlying auxin regulation of growth, challenging several existing models. We focus on the divergent mechanisms of apoplastic pH regulation in shoots and roots revisiting the classical Acid Growth Theory and discuss coordinated involvement of multiple auxin signaling pathways. From this emerges a more comprehensive, updated picture how auxin regulates growth."
Authors: Colin P. S. Kruse and Sarah E. Wyatt.
Plant Science (2022)
Highlights: • An extensive literature meta-analysis in the context of published RNA and protein expression data has allowed for the assembly of a cohesive schematic of gravity signaling pathways. • Nitric oxide signaling (opposed by ethylene) and the actions of reactive oxygen species are central to the signaling elements integrated by the schematic. • The causal links between schematic signaling components fits existing physiological data in Arabidopsis roots (the most well studied gravity-sensing tissue in plants). • The conservation of S-nitrosation events relevant to the schematic provides insights into the evolutionary pressures for retention of nitric oxide signaling events in schematic pathways and indicates a potential for use of these pathways in other tropic cascades.
Abstract: "Plant signaling components are often involved in numerous processes. Calcium, reactive oxygen species, and other signaling molecules are essential to normal biotic and abiotic responses. Yet, the summation of these components is integrated to produce a specific response despite their involvement in a myriad of response cascades. In the response to gravity, the role of many of these individual components has been studied, but a specific sequence of signals has not yet been assembled into a cohesive schematic of gravity response signaling. Herein, we provide a review of existing knowledge of gravity response and differential protein and gene regulation induced by the absence of gravity stimulus aboard the International Space Station and propose an integrated theoretical schematic of gravity response incorporating that information. Recent developments in the role of nitric oxide in gravity signaling provided some of the final contextual pillars for the assembly of the model, where nitric oxide and the role of cysteine S-nitrosation may be central to the gravity response. The proposed schematic accounts for the known responses to reorientation with respect to gravity in roots—the most well studied gravitropic plant tissue—and is supported by the extensive evolutionary conservation of regulatory amino acids within protein components of the signaling schematic. The identification of a role of nitric oxide in regulating the TIR1 auxin receptor is indicative of the broader relevance of the schematic in studying a multitude of environmental and stress responses. Finally, there are several experimental approaches that are highlighted as essential to the further study and validation of this schematic."
Authors: Lanxin Li, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez, Jack Merrin, Jian Chen, Lana Shabala, Wouter Smet, Hong Ren, Steffen Vanneste, Sergey Shabala, Bert De Rybel, Dolf Weijers, Toshinori Kinoshita, William M. Gray and Jiří Friml.
Nature (2021)
One-sentence summary: Auxin rapidly modulates root growth through simultaneous activation of two opposing mechanisms—TMK1-mediated apoplast acidification and TIR1/AFB-mediated apoplast alkalinization.
Abstract: "Growth regulation tailors development in plants to their environment. A prominent example of this is the response to gravity, in which shoots bend up and roots bend down1. This paradox is based on opposite effects of the phytohormone auxin, which promotes cell expansion in shoots while inhibiting it in roots via a yet unknown cellular mechanism2. Here, by combining microfluidics, live imaging, genetic engineering and phosphoproteomics in Arabidopsis thaliana, we advance understanding of how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on rapid regulation of apoplastic pH, a causative determinant of growth. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular canonical auxin signalling promotes net cellular H+ influx, causing apoplast alkalinization. Simultaneous activation of these two counteracting mechanisms poises roots for rapid, fine-tuned growth modulation in navigating complex soil environments."
Author: M. Arif Ashraf
Molecular Plant (2021)
Excerpts: "Upon activation, the PIEZO channel facilitates the entry of Ca2+ inside the cell (Figure 1), which translates into both short-term cellular signals by altering the ion concentrations and long-term cellular signals by regulating gene expression (Parpaite and Coste, 2017). The sequences of PIEZO family proteins are highly conserved in vertebrates, plants, and protozoa, but the function of PIEZOs in plants remain unclear. In a recent study, Radin et al. (2021) investigated the role of PIEZOs in the moss Physcomitrium patens and higher plant Arabidopsis thaliana."
"Despite the similar functionality to animal counterparts for Ca2+ oscillation (Coste et al., 2010), moss PIEZOs are localized in the tonoplast, in contrast to the plasma membrane localization of animal PIEZOs (Figure 1)"
"They also produced the loss-of-function mutants of AtPIEZO1 (atpiezo1-9, atpiezo1-10) using the CRISPR/Cas9 system and found that these Arabidopsis mutants display the expanded vacuolar phenotype in the pollen tubes. Collectively, the study by Radin et al. (2021) suggest a conserved function of PIEZOs as mechanosensory proteins in land plants."
Authors: Dimitris Templalexis, Dikran Tsitsekian, Chen Liu, Gerasimos Daras, Jan Šimura, Panagiotis Moschou, Karin Ljung, Polydefkis Hatzopoulos and Stamatis Rigas.
Plant Physiology (2022)
Abstract: "In plants, auxin transport and development are tightly coupled, just as hormone and growth responses are intimately linked in multicellular systems. Here we provide insights into uncoupling this tight control by specifically targeting the expression of TINY ROOT HAIR 1 (TRH1), a member of plant HAK/KUP/KT transporters that facilitate potassium uptake by co-transporting protons, in Arabidopsis root cell files. Use of this system pinpointed specific root developmental responses to acropetal versus basipetal auxin transport. Loss of TRH1 function shows tiny root hairs and defective root gravitropism, associated with auxin imbalance in the root apex. Cell file-specific expression of TRH1 in the central cylinder rescued trh1 root agravitropism, whereas positional TRH1 expression in peripheral cell layers, including epidermis and cortex, restored trh1 root hair defects. Applying a systems-level approach, the role of RAP2.11 and RSL5 transcription factors in root hair development was verified. Furthermore, ERF53 and WRKY51 transcription factors were overrepresented upon restoration of root gravitropism supporting involvement in gravitropic control. Auxin has a central role in shaping root system architecture by regulating multiple developmental processes. We reveal that TRH1 jointly modulates intracellular ionic gradients and cell-to-cell polar auxin transport to drive root epidermal cell differentiation and gravitropic response. Our results indicate the developmental importance of HAK/KUP/KT proton-coupled K+ transporters.
Author: Markus M. Geisler.
Frontiers in Plant Science (2021)
Introduction: "The transport of the plant hormone auxin has been a hotspot in plant biology since its discovery (Darwin and Darwin, 1880; Zazimalova et al., 2010; Friml, 2021; Hammes et al., 2021). After its identification and verification as IAA (3-indolyl acetic acid; Went and Thimann, 1937), auxin gained high interest and fascination in the plant community but also in society because it allowed us to explain daily-seen phenomena, such as phototropism, gravitropism, patterning, and development (Christie and Murphy, 2013; Geisler et al., 2014; Morohashi et al., 2017; Konstantinova et al., 2021). The mid twentieth century saw the emergence in the use of artificial and natural auxins as growth regulators and herbicides, and led to advances in reduced tillage agriculture as well as widespread military use of “auxinic” defoliants, such as 2,4-D (Friml and Palme, 2002). This first major wave of auxin research characterized by a predominantly biochemical characterization of auxin action in respect to growth lasted until the early 1990's and resulted in fascinating concepts, including the “chemiosmotic model of auxin transport” (Rubery and Sheldrake, 1973, 1974; Raven, 1975; Goldsmith, 1977; see Figure 1) and the “auxin canalization theory” (Sachs, 2000; Bennett et al., 2014; Ravichandran et al., 2020)."
Authors: Hyodong Lee, Anindya Ganguly, Song Baik and Hyung-Taeg Cho.
The Plant Cell (2021)
Abstract: "PIN-FORMED (PIN)-mediated polar auxin transport is involved in key developmental processes in plants. Various internal and external cues influence plant development via the modulation of intracellular PIN polarity and, thus, the direction of polar auxin transport, but the mechanisms underlying these processes remain largely unknown. PIN proteins harbor a hydrophilic loop (HL) that has important regulatory functions; here, we used the HL as bait in protein pulldown screening for modulators of intracellular PIN trafficking in Arabidopsis thaliana. CPK29, a Ca2+-dependent protein kinase, was identified and shown to phosphorylate specific target residues on the PIN-HL that were not phosphorylated by other kinases. Furthermore, loss of CPK29 or mutations of the phospho-target residues in PIN-HLs significantly compromised intracellular PIN trafficking and polarity, causing defects in PIN-mediated auxin redistribution and biological processes such as lateral root formation, root twisting, hypocotyl gravitropism, phyllotaxis, and reproductive development. These findings indicate that CPK29 directly interprets Ca2+ signals from internal and external triggers, resulting in the modulation of PIN trafficking and auxin responses."
Authors: Sonhita Chakraborty, Masatsugu Toyota, Wolfgang Moeder, Kimberley Chin, Alex Fortuna, Marc Champigny, Steffen Vanneste, Simon Gilroy, Tom Beeckman, Eiji Nambara and Keiko Yoshioka.
Plant Physiology (2021)
Abstract: "Cyclic Nucleotide Gated Ion Channels (CNGCs) have been firmly established as Ca2+-conducting ion channels that regulate a wide variety of physiological responses in plants. CNGC2 has been implicated in plant immunity and Ca2+ signaling due to the autoimmune phenotypes exhibited by null mutants of CNGC2 in Arabidopsis thaliana. However, cngc2 mutants display additional phenotypes that are unique among autoimmune mutants, suggesting that CNGC2 has functions beyond defense and generates distinct Ca2+ signals in response to different triggers. In this study we found that cngc2 mutants showed reduced gravitropism, consistent with a defect in auxin signaling. This was mirrored in the diminished auxin response detected by the auxin reporters DR5::GUS and DII-VENUS and in a strongly impaired auxin-induced Ca2+ response. Moreover, the cngc2 mutant exhibits higher levels of the endogenous auxin indole-3-acetic acid (IAA), indicating that excess auxin in the cngc2 mutant causes its pleiotropic phenotypes. These auxin signaling defects and the autoimmunity syndrome of the cngc2 mutant could be suppressed by loss-of-function mutations in the auxin biosynthesis gene YUCCA6 (YUC6), as determined by identification of the cngc2 suppressor mutant repressor of cngc2 (rdd1) as an allele of YUC6. A loss-of-function mutation in the upstream auxin biosynthesis gene TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA1, WEAK ETHYLENE INSENSITIVE8) also suppressed the cngc2 phenotypes, further supporting the tight relationship between CNGC2 and the TAA–YUC-dependent auxin biosynthesis pathway. Taking these results together, we propose that the Ca2+ signal generated by CNGC2 is a part of the negative feedback regulation of auxin homeostasis in which CNGC2 balances cellular auxin perception by influencing auxin biosynthesis."
Authors: Huibin Han, Maciek Adamowski, Linlin Qi, Saqer S. Alotaibi and Jiří Friml.
New Phytologist (2021)
Abstract: "Tropisms, growth responses to environmental stimuli such as light or gravity, are spectacular examples of adaptive plant development. The plant hormone auxin serves as a major coordinative signal. The PIN auxin exporters, through their dynamic polar subcellular localizations, redirect auxin fluxes in response to environmental stimuli and the resulting auxin gradients across organs underlie differential cell elongation and bending. In this review, we discuss recent advances concerning regulations of PIN polarity during tropisms, focusing on PIN phosphorylation and trafficking. We also cover how environmental cues regulate PIN actions during tropisms, and a crucial role of auxin feedback on PIN polarity during bending termination. Finally, the interactions between different tropisms are reviewed to understand plant adaptive growth in the natural environment."
Authors: Linzhou Huang, Wenguang Wang, Ning Zhang, Yueyue Cai, Yan Liang, Xiangbing Meng, Yundong Yuan, Jiayang Li, Dianxing Wu and Yonghong Wang.
New Phytologist (2021)
Abstract: "Rice (Oryza sativa) tiller angle is a key component for achieving ideal plant architecture and higher grain yield. However, the molecular mechanism underlying rice tiller angle remains elusive. We characterized a novel rice tiller angle mutant lazy2 (la2) and isolated the causative gene LA2 through map-based cloning. Biochemical, molecular and genetic studies were conducted to elucidate the LA2-involved tiller angle regulatory mechanism. The la2 mutant shows large tiller angle with impaired shoot gravitropism and defective asymmetric distribution of auxin. We found that starch granules in amyloplasts are completely lost in the gravity-sensing leaf sheath base cells of la2, whereas the seed development is not affected. LA2 encodes a novel chloroplastic protein that can interact with the starch biosynthetic enzyme Oryza sativa plastidic phosphoglucomutase (OspPGM) to regulate starch biosynthesis in rice shoot gravity-sensing cells. Genetic analysis showed that LA2 regulates shoot gravitropism and tiller angle by acting upstream of LA1 to mediate lateral auxin transport. Our studies revealed that LA2 acts as a novel regulator of rice tiller angle by specifically regulating starch biosynthesis in gravity-sensing cells, and established the framework of the starch-statolith-dependent rice tiller angle regulatory pathway, providing new insights into the rice tiller angle regulatory network."
Authors: Bruno Moulia, Stéphane Douady and Olivier Hamant.
Science (2021)
Editor's view: Plant proprioception - Plants are battered inside and out by mechanical forces such as gravity, wind, or a passerby plucking a flower. Moulia et al. review what is known about how plants sense and interpret mechanical forces to guide growth and development. Minute fluctuations in mechanical cues form the basis of a developmental proprioception system that ensures steady growth despite variable environments.
Abstract: "Plants constantly experience fluctuating internal and external mechanical cues, ranging from nanoscale deformation of wall components, cell growth variability, nutating stems, and fluttering leaves to stem flexion under tree weight and wind drag. Developing plants use such fluctuations to monitor and channel their own shape and growth through a form of proprioception. Fluctuations in mechanical cues may also be actively enhanced, producing oscillating behaviors in tissues. For example, proprioception through leaf nastic movements may promote organ flattening. We propose that fluctuation-enhanced proprioception allows plant organs to sense their own shapes and behave like active materials with adaptable outputs to face variable environments, whether internal or external. Because certain shapes are more amenable to fluctuations, proprioception may also help plant shapes to reach self-organized criticality to support such adaptability."
Authors: Rui Miao, Wei Yuan, Yue Wang, Irene Garcia-Maquilon, Xiaolin Dang, Ying Li, Jianhua Zhang, Yiyong Zhu, Pedro L. Rodriguez and Weifeng Xu.
Science Advances (2021)
Abstract: "The hab1-1abi1-2abi2-2pp2ca-1 quadruple mutant (Qabi2-2) seedlings lacking key negative regulators of ABA signaling, namely, clade A protein phosphatases type 2C (PP2Cs), show more apoplastic H+ efflux in roots and display an enhanced root growth under normal medium or water stress medium compared to the wild type. The presence of low ABA concentration (0.1 micromolar), inhibiting PP2C activity via monomeric ABA receptors, enhances root apoplastic H+ efflux and growth of the wild type, resembling the Qabi2-2 phenotype in normal medium. Qabi2-2 seedlings also demonstrate increased hydrotropism compared to the wild type in obliquely-oriented hydrotropic experimental system, and asymmetric H+ efflux in root elongation zone is crucial for root hydrotropism. Moreover, we reveal that Arabidopsis ABA-insensitive 1, a key PP2C in ABA signaling, interacts directly with the C terminus of Arabidopsis plasma membrane H+-dependent adenosine triphosphatase 2 (AHA2) and dephosphorylates its penultimate threonine residue (Thr947), whose dephosphorylation negatively regulates AHA2."
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Authors: Bruno Moulia, Eric Badel, Renaud Bastien, Laurent Duchemin and Christophe Eloy.
New Phytologist (2022)
Abstract: "Shoot morphogenetic plasticity is crucial to the adaptation of plants to their fluctuating environments. Major insights into shoot morphogenesis have been compiled studying meristems, especially the shoot apical meristem (SAM), through a methodological effort in multiscale systems biology and biophysics. However, morphogenesis at the SAM is robust to environmental changes. Plasticity emerges later on during post-SAM development. The purpose of this review is to show that multiscale systems biology and biophysics is insightful for the shaping of the whole plant as well. More specifically, we review the shaping of axes and crowns through tropisms and elasticity, combining the recent advances in morphogenetic control using physical cues and by genes. We focus mostly on land angiosperms, but with growth habits ranging from small herbs to big trees. We show that generic (universal) morphogenetic processes have been identified, revealing feedforward and feedback effects of global shape on the local morphogenetic process. In parallel, major advances have been made in the analysis of the major genes involved in shaping axes and crowns, revealing conserved genic networks among angiosperms. Then, we show that these two approaches are now starting to converge, revealing exciting perspectives."
Abstract: Luis Morales-Quintana and Patricio Ramos.
International Journal of Molecular Sciences (2021)
Abstract: "Plants reorient the growth of affected organs in response to the loss of gravity vector. In trees, this phenomenon has received special attention due to its importance for the forestry industry of conifer species. Sustainable management is a key factor in improving wood quality. It is of paramount importance to understand the molecular and genetic mechanisms underlying wood formation, together with the hormonal and environmental factors that affect wood formation and quality. Hormones are related to the modulation of vertical growth rectification. Many studies have resulted in a model that proposes differential growth in the stem due to unequal auxin and jasmonate allocation. Furthermore, many studies have suggested that in auxin distribution, flavonoids act as molecular controllers. It is well known that flavonoids affect auxin flux, and this is a new area of study to understand the intracellular concentrations and how these compounds can control the gravitropic response. In this review, we focused on different molecular aspects related to the hormonal role in flavonoid homeostasis and what has been done in conifer trees to identify molecular players that could take part during the gravitropic response and reduce low-quality wood formation."
Author: Marc Somssich.
Plant Physiology (2022)
Excerpts: "Root hair growth is also influenced by auxin, in this case by auxin transported towards the shoot in the root epidermis cells. TINY ROOT HAIR 1 (TRH1) is a potassium transporter initially identified for its root hair mutant phenotype (Rigas et al., 2001)."
"In the current issue of Plant Physiology, the team of Stamatis Rigas reveals how TRH1 contributes to auxin distribution in the root apex in a cell-type specific manner, thereby influencing the root’s gravitropic response and hair cell differentiation (Templalexis et al., 2021)."
"The work presented by Templalexis et al indicates that TRH1 supports auxin efflux to maintain correct auxin distribution and proper development of the root. TRH1 is expressed throughout the root tip and therefore supports auxin transport towards the root tip, as well as upwards toward the shoot. Accordingly, the two trh1 mutant phenotypes analyzed here can be either attributed to impaired downwards transport (gravitropism), or impaired upwards transport (root hair development) (Figure 1B)."
Authors: Chaohui Ding, Xianhui Lin, Ying Zuo, Zhilin Yu, Scott R. Baerson, Zhiqiang Pan, Rensen Zeng and Yuanyuan Song.
The Plant Journal (2021)
Abstract: "Tiller angle is an important determinant of plant architecture in rice (Oryza sativa L.). Auxins play a critical role in determining plant architecture; however, the underlying metabolic and signaling mechanisms are still largely unknown. In this study, we have identified a member of the bZIP family of TGA class transcription factors, OsbZIP49, that participates in the regulation of plant architecture and is specifically expressed in gravity-sensing tissues, including the shoot base, nodes and lamina joints. Transgenic rice plants overexpressing OsbZIP49 displayed a tiller-spreading phenotype with reduced plant height and internode lengths. In contrast, CRISPR/Cas9-mediated knockout of OsbZIP49 resulted in a compact architecture. Follow-up studies indicated that the effects of OsbZIP49 on tiller angles are mediated through changes in shoot gravitropic responses. Additionally, we provide evidence that OsbZIP49 activates the expression of indole-3-acetic acid-amido synthetases OsGH3-2 and OsGH3-13 by directly binding to TGACG motifs located within the promoters of both genes. Increased GH3-catalyzed conjugation of indole-3-acetic acid (IAA) in rice transformants overexpressing OsbZIP49 resulted in the increased accumulation of IAA-Asp and IAA-Glu, and a reduction in local free auxin, tryptamine and IAA-Glc levels. Exogenous IAA or naphthylacetic acid (NAA) partially restored shoot gravitropic responses in OsbZIP49-overexpressing plants. Knockout of OsbZIP49 led to reduced expression of both OsGH3-2 and OsGH3-13 within the shoot base, and increased accumulation of IAA and increased OsIAA20 expression levels were observed in transformants following gravistimulation. Taken together, the present results reveal the role transcription factor OsbZIP49 plays in determining plant architecture, primarily due to its influence on local auxin homeostasis."
Authors: Ivan Kashkan, Mónika Hrtyan, Katarzyna Retzer, Jana Humpolíčková, Aswathy Jayasree, Roberta Filepová ,Zuzana Vondráková, Sibu Simon, Debbie Rombaut, Thomas B. Jacobs, Mikko J. Frilander, Jan Hejátko, Jiří Friml, Jan Petrášek and Kamil Růžička.
New Phytologist (2022)
Abstract: "Advanced transcriptome sequencing has uncovered that the majority of eukaryotic genes undergo alternative splicing (AS). Nonetheless, little effort has been dedicated to investigating the functional relevance of particular splicing events, even those in the key developmental and hormonal regulators. Combining approaches of genetics, biochemistry and advanced confocal microscopy, we describe the impact of alternative splicing on the PIN7 gene in the plant model Arabidopsis thaliana. PIN7 encodes a polarly localized transporter for the phytohormone auxin and produces two evolutionary-conserved transcripts PIN7a and PIN7b. PIN7a and PIN7b, differing in a 4-amino acid motif, exhibit almost identical expression pattern and subcellular localization. We reveal that they closely associate and mutually influence their mobility within the plasma membrane. Phenotypic complementation tests indicate that the functional contribution of PIN7b per se is minor, but it markedly reduces the prominent PIN7a activity, which is required for correct seedling apical hook formation and auxin-mediated tropic responses. Our results establish alternative splicing of the PIN family as a conserved, functionally relevant mechanism, unveiling an additional regulatory level of auxin-mediated plant development."
Authors: Ying Liu and Nicolaus von Wirén.
Current Opinion in Plant Biology (2022)
Abstract: "In most soils, the spatial distribution of nutrients and water in the rooting zone of plants is heterogeneous and changes over time. To access localized resources more efficiently, plants induce foraging responses by modulating individual morphological root traits, such as the length of the primary root or the number and length of lateral roots. These adaptive responses require the integration of exogenous and endogenous nutrient- or water-related signals into the root developmental program. Recent studies corroborated a central role of auxin in shaping root architectural traits in response to fluctuating nutrient and water availabilities. In this review, we highlight current knowledge on nutrient- and water-related developmental processes that impact root foraging and involve auxin as a central player. A deeper understanding and exploitation of these auxin-related processes and mechanisms promises advances in crop breeding for higher resource efficiency."
Authors: Maddalena Salvalaio, Nicholas Oliver, Deniz Tiknaz, Maximillian Schwarze, Nicolas Kral, Soo-Jeong Kim and Giovanni Sena.
bioRxiv (2021)
Abstract: "An efficient foraging strategy for plant roots relies on the ability to sense multiple physical and chemical cues in soil and to reorient growth accordingly (tropism). Root tropisms range from sensing gravity (gravitropism), light (phototropism), water (hydrotropism), touch (thigmotropism) and more. Electrotropism, also known as galvanotropism, is the phenomenon of aligning growth with external electric fields and currents. Although observed in a few species since the end of the 19th century, the molecular and physical mechanism of root electrotropism remains elusive, limiting the comparison to more defined sensing pathways in plants. Here we provide a first quantitative and molecular characterisation of root electrotropism in the model system Arabidopsis thaliana, showing that it does not depend on an asymmetric distribution of the plant hormone auxin, but that instead it requires the biosynthesis of a second hormone, cytokinin. We also show that the dose-response kinetics of the early steps of root electrotropism follows a power law analogous to the one observed in some physiological reactions in animals. A future full molecular and quantitative characterisation of root electrotropism would represent a step forward towards a better understanding of signal integration in plants, and an independent outgroup for comparative analysis of electroreception in animals and fungi."
Authors: Andrea Chini, Isabel Monte, Gemma Fernández-Barbero, Marta Boter, Glenn Hicks, Natasha Raikhel and Roberto Solano.
Plant Physiology (2021)
Abstract: "The phytohormone JA-Ile regulates many stress responses and developmental processes in plants. A co-receptor complex formed by the F-box protein COI1 (Coronatine Insensitive 1) and a JAZ (Jasmonate ZIM-domain) repressor perceives the hormone. JA-Ile antagonists are invaluable tools for exploring the role of JA-Ile in specific tissues and developmental stages, and for identifying regulatory processes of the signalling pathway. Using two complementary chemical screens, we identified three compounds that exhibit a robust inhibitory effect on both the hormone-mediated COI-JAZ interaction and degradation of JAZ1 and JAZ9 in vivo. One molecule, J4, also restrains specific JA-induced physiological responses in different angiosperm plants, including JA-mediated gene expression, growth inhibition, chlorophyll degradation and anthocyanin accumulation. Interaction experiments with purified proteins indicate that J4 directly interferes with the formation of the Arabidopsis (Arabidopsis thaliana) COI1-JAZ complex otherwise induced by JA. The antagonistic effect of J4 on COI1-JAZ also occurs in the liverwort Marchantia polymorpha, suggesting the mode of action is conserved in land plants. Besides JA signalling, J4 works as an antagonist of the closely-related auxin signalling pathway, preventing TIR1/Aux-IAA interaction and auxin responses in planta, including hormone-mediated degradation of an auxin repressor, gene expression and gravitropic response. However, J4 does not affect other hormonal pathways. Altogether, our results show that this dual antagonist competes with JA-Ile and auxin, preventing the formation of phylogenetically related receptor complexes. J4 may be a useful tool to dissect both the JA-Ile and auxin pathways in particular tissues and developmental stages since it reversibly inhibits these pathways."
Authors: Nelson B. C. Serre, Dominik Kralík, Ping Yun, Zdeněk Slouka, Sergey Shabala and Matyáš Fendrych.
Nature Plants (2021)
One-sentence summary: A probe to visualize membrane potential in real time is used to connect rapid auxin-induced membrane depolarization with root growth inhibition, which are both controlled by the AFB1 auxin receptor.
Abstract: "The membrane potential reflects the difference between cytoplasmic and apoplastic electrical potentials and is essential for cellular operation. The application of the phytohormone auxin (3-indoleacetic acid (IAA)) causes instantaneous membrane depolarization in various cell types1,2,3,4,5,6, making depolarization a hallmark of IAA-induced rapid responses. In root hairs, depolarization requires functional IAA transport and TIR1–AFB signalling5, but its physiological importance is not understood. Specifically in roots, auxin triggers rapid growth inhibition7,8,9 (RGI), a process required for gravitropic bending. RGI is initiated by the TIR1–AFB co-receptors, with the AFB1 paralogue playing a crucial role10,11. The nature of the underlying rapid signalling is unknown, as well as the molecular machinery executing it. Even though the growth and depolarization responses to auxin show remarkable similarities, the importance of membrane depolarization for root growth inhibition and gravitropism is unclear. Here, by combining the DISBAC2(3) voltage sensor with microfluidics and vertical-stage microscopy, we show that rapid auxin-induced membrane depolarization tightly correlates with RGI. Rapid depolarization and RGI require the AFB1 auxin co-receptor. Finally, AFB1 is essential for the rapid formation of the membrane depolarization gradient across the gravistimulated root. These results clarify the role of AFB1 as the central receptor for rapid auxin responses."
Authors: Jin-dong Zhu, Jing Wang, Xi-ning Guo, Bao-shuan Shang, Hong-ru Yan, Xiao Zhang and Xiang Zhao.
Journal of Experimental Botany (2021)
Abstract: "Hypocotyl phototropism is mediated by the phototropins and plays a critical role in seedling morphogenesis by optimizing growth orientation. However, the mechanisms by which phototropism influences morphogenesis require additional study, especially for polyploid crops such as cotton. Here, we found that hypocotyl phototropism was weaker in G. arboreum than in G. raimondii (two diploid cotton species), and LC-MS analysis indicated that G. arboreum hypocotyls had a higher content of ABA and a lower content of IAA and bioactive GAs. Consistently, the expression of ABA2, AAO3 and GA2OX1 was higher in G. arboreum than in G. raimondii, and that of GA3OX was lower; these changes promoted ABA synthesis and the transformation of active GA to inactive GA. Higher concentrations of ABA inhibited the asymmetric distribution of IAA across the hypocotyl and blocked the phototropic curvature of G. raimondii. Application of IAA or GA3 to the shaded and illuminated sides of the hypocotyl enhanced and inhibited phototropic curvature, respectively, in G. arboreum. The application of IAA but not GA to one side of the hypocotyl caused hypocotyl curvature in the dark. These results indicate that the asymmetric distribution of IAA promotes phototropic growth, and the weakened phototropic curvature of G. arboreum may be attributed to its higher ABA levels that inhibit the action of auxin, which is regulated by GA signaling."
Authors: Despina Samakovli, Loukia Roka, Anastasia Dimopoulou, Panagiota Konstantinia Plitsi, Asta Žukauskaitė, Paraskevi Georgopoulou, Ondřej Novák, Dimitra Milioni and Polydefkis Hatzopoulos.
New Phytologist (2021)
Abstract: "Auxin homeostasis and signaling affect a broad range of developmental processes in plants. The interplay between HSP90 and auxin signaling is channeled through the chaperoning capacity of the HSP90 on the TIR1 auxin receptor. The sophisticated buffering capacity of the HSP90 system through the interaction with diverse signaling protein components drastically shapes genetic circuitries regulating various developmental aspects. However, the elegant networking capacity of HSP90 in the global regulation of auxin response and homeostasis has not been appreciated. Arabidopsis hsp90 mutants were screened for gravity response. Phenotypic analysis of root meristems and cotyledon veins was performed. PIN1 localization in hsp90 mutants was determined. Our results showed that HSP90 affected the asymmetrical distribution of PIN1 in plasma membranes and influenced its expression in prompt cell niches. Depletion of HSP90 distorted polar distribution of auxin, as the acropetal auxin transport was highly affected, leading to impaired root gravitropism and lateral root formation. The essential role of the HSP90 in auxin homeostasis was profoundly evident from early development, as HSP90 depletion affected embryo development and the pattern formation of veins in cotyledons. Our data suggest that the HSP90-mediated distribution of PIN1 modulates auxin distribution and thereby auxin signaling to properly promote plant development."
Authors: Nicolas Levernier, Olivier Pouliquen and Yoël Forterre.
Frontiers in Plant Science (2021)
Abstract: "Gravity is a major cue for the proper growth and development of plants. The response of plants to gravity implies starch-filled plastids, the statoliths, which sediments at the bottom of the gravisensing cells, the statocytes. Statoliths are assumed to modify the transport of the growth hormone, auxin, by acting on specific auxin transporters, PIN proteins. However, the complete gravitropic signaling pathway from the intracellular signal associated to statoliths to the plant bending is still not well-understood. In this article, we build on recent experimental results showing that statoliths do not act as gravitational force sensor, but as position sensor, to develop a bottom-up theory of plant gravitropism. The main hypothesis of the model is that the presence of statoliths modifies PIN trafficking close to the cell membrane. This basic assumption, coupled with auxin transport and growth in an idealized tissue made of a one-dimensional array of cells, recovers several major features of the gravitropic response of plants. First, the model provides a new interpretation for the response of a plant to a steady stimulus, the so-called sine-law of plant gravitropism. Second, it predicts the existence of a gravity-independent memory process as observed recently in experiments studying the response to transient stimulus. The model suggests that the timescale of this process is associated to PIN turnover, calling for new experimental studies."
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