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Authors: M. Arif Ashraf and Dior R. Kelley.
Molecular Plant (2021)
Excerpts: "A recent study from Jiri Friml's group used both genetic and microscopic approaches to identify a novel receptor kinase module that functions in PIN-dependent auxin transport during canalization (Hajný et al., 2020)."
"This led the authors to propose a model for depicting the role of CAMEL-mediated phosphorylation of PIN1: post-translational modification of PIN1 is required for auxin-mediated PIN repolarization and thus for establishment of directional auxin channels (Figure 1). The identification of the CAMEL–CANAR module provided a major advance in understanding how PIN-dependent auxin transport is controlled during canalization."
Authors: Junzhe Wang, Xiaolong Guo, Qiang Xiao, Jianchu Zhu, Alice Y. Cheung, Li Yuan, Elizabeth Vierling and Shengbao Xu.
New Phytologist (2021)
Abstract: "The nucellus tissue in flowering plants provides nutrition for the development of the female gametophyte (FG) and young embryo. The nucellus degenerates as the FG develops, but the mechanism controlling the coupled process of nucellar degeneration and FG expansion remains largely unknown. The degeneration process of the nucellus and spatiotemporal auxin distribution in the developing ovule before fertilization were investigated in Arabidopsis thaliana. Nucellar degeneration before fertilization occurs through vacuolar cell death and in a ordered degeneration fashion. This sequential nucellar degeneration is controlled by the signalling molecule auxin. Auxin efflux plays the core role in precisely controlling the spatiotemporal pattern of auxin distribution in the nucellus surrounding the FG. The auxin efflux carrier PIN1 transports maternal auxin into the nucellus while PIN3/PIN4/PIN7 further delivers auxin to degenerating nucellar cells and concurrently controls FG central vacuole expansion. Notably, auxin level and auxin efflux are controlled by the maternal tissues, acting as a key communication from maternal to filial tissue."
Authors: Yuzhou Zhang, Lesia Rodriguez, Lanxin Li, Xixi Zhang and Jiří Friml.
Science Advances (2020)
Abstract: "Flowering plants display the highest diversity among plant species and have notably shaped terrestrial landscapes. Nonetheless, the evolutionary origin of their unprecedented morphological complexity remains largely an enigma. Here, we show that the coevolution of cis-regulatory and coding regions of PIN-FORMED (PIN) auxin transporters confined their expression to certain cell types and directed their subcellular localization to particular cell sides, which together enabled dynamic auxin gradients across tissues critical to the complex architecture of flowering plants. Extensive intraspecies and interspecies genetic complementation experiments with PINs from green alga up to flowering plant lineages showed that PIN genes underwent three subsequent, critical evolutionary innovations and thus acquired a triple function to regulate the development of three essential components of the flowering plant Arabidopsis: shoot/root, inflorescence, and floral organ. Our work highlights the critical role of functional innovations within the PIN gene family as essential prerequisites for the origin of flowering plants."
Authors: Li Ping Tang, Yi Yang, Hui Wang, Lixin Li, Le Liu, Yu Liu, Jinfeng Yuan, Xiang Yu Zhao, Klaus Palme, Ying Hua Su and Xugang Li.
Journal of Integrative Plant Biology (2020)
Abstract: "In eukaryotes, N‐ethylmaleimide‐sensitive factor (NSF) is a conserved AAA+ ATPase and a key component of the membrane trafficking machinery that promotes the fusion of secretory vesicles with target membranes. Here, we demonstrate that the Arabidopsis thaliana genome contains a single copy of NSF, AtNSF, which plays an essential role in the regulation of leaf serration. The AtNSF knock‐down mutant, atnsf‐1, exhibited more serrations in the leaf margin. Moreover, polar localization of the PIN‐FORMED1 (PIN1) auxin efflux transporter was diffuse around the margins of atnsf‐1 leaves and root growth was inhibited in the atnsf‐1 mutant. More PIN1‐GFP accumulated in the intracellular compartments of atnsf‐1 plants, suggesting that AtNSF is required for intracellular trafficking of PIN between the endosome and plasma membrane. Furthermore, the serration phenotype was suppressed in the atnsf‐1 pin1‐8 double mutant, suggesting that AtNSF is required for PIN1‐mediated polar auxin transport to regulate leaf serration. The CUP‐SHAPED COTYLEDON2 (CUC2) transcription factor gene is up‐regulated in atnsf‐1 plants and the cuc2‐3 single mutant exhibits smooth leaf margins, demonstrating that AtNSF also functions in the CUC2 pathway. Our results reveal that AtNSF regulates the PIN1‐generated auxin maxima with a CUC2‐mediated feedback loop to control leaf serration."
Authors: Shutang Tan, Martin Di Donato, Matouš Glanc, Xixi Zhang, Petr Klíma, Jie Liu, Aurélien Bailly, Noel Ferro, Jan Petrášek, Markus Geisler and Jiří Friml.
Cell Reports (2020)
Highlights: • NSAIDs exhibit striking activity in shaping Arabidopsis root development • NSAIDs interfere with auxin transport and endomembrane trafficking • NSAID treatments impair actin filament dynamics and endosomal mobility • NSAIDs directly target TWD1, suppressing its chaperone activity and actin dynamics
Abstract: "The widely used non-steroidal anti-inflammatory drugs (NSAIDs) are derivatives of the phytohormone salicylic acid (SA). SA is well known to regulate plant immunity and development, whereas there have been few reports focusing on the effects of NSAIDs in plants. Our studies here reveal that NSAIDs exhibit largely overlapping physiological activities to SA in the model plant Arabidopsis. NSAID treatments lead to shorter and agravitropic primary roots and inhibited lateral root organogenesis. Notably, in addition to the SA-like action, which in roots involves binding to the protein phosphatase 2A (PP2A), NSAIDs also exhibit PP2A-independent effects. Cell biological and biochemical analyses reveal that many NSAIDs bind directly to and inhibit the chaperone activity of TWISTED DWARF1, thereby regulating actin cytoskeleton dynamics and subsequent endosomal trafficking. Our findings uncover an unexpected bioactivity of human pharmaceuticals in plants and provide insights into the molecular mechanism underlying the cellular action of this class of anti-inflammatory compounds."
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Authors: Lindy Abas, Martina Kolb, Johannes Stadlmann, Dorina P. Janacek, Kristina Lukic, Claus Schwechheimer, Leonid A. Sazanov, Lukas Mach, Jiří Friml, and Ulrich Z. Hammes.
PNAS (2021)
Significance: The plant hormone auxin regulates many aspects of plant life and has the unique ability to flow throughout the plant in defined directions, as observed by Darwin over a century ago. The chemical NPA inhibits this directional flow, thereby severely affecting plant growth. In studying the specific effects of NPA, researchers have also uncovered general principles underlying plant development. Exactly how NPA inhibits directional auxin flow is unclear. NPA interacts with proteins that can transport auxin, such as ABCB transporters, and we show here that NPA also associates with and inhibits the major transporters that specialize in directional auxin flow—PINs. This explanation of NPA action will guide future research and may help reveal how PINs perform auxin transport.
Abstract: "N-1-naphthylphthalamic acid (NPA) is a key inhibitor of directional (polar) transport of the hormone auxin in plants. For decades, it has been a pivotal tool in elucidating the unique polar auxin transport-based processes underlying plant growth and development. Its exact mode of action has long been sought after and is still being debated, with prevailing mechanistic schemes describing only indirect connections between NPA and the main transporters responsible for directional transport, namely PIN auxin exporters. Here we present data supporting a model in which NPA associates with PINs in a more direct manner than hitherto postulated. We show that NPA inhibits PIN activity in a heterologous oocyte system and that expression of NPA-sensitive PINs in plant, yeast, and oocyte membranes leads to specific saturable NPA binding. We thus propose that PINs are a bona fide NPA target. This offers a straightforward molecular basis for NPA inhibition of PIN-dependent auxin transport and a logical parsimonious explanation for the known physiological effects of NPA on plant growth, as well as an alternative hypothesis to interpret past and future results. We also introduce PIN dimerization and describe an effect of NPA on this, suggesting that NPA binding could be exploited to gain insights into structural aspects of PINs related to their transport mechanism."
Authors: Zhicheng Jiao, Huan Du, Shu Chen, Wei Huang and Liangfa Ge.
Frontiers in Plant Science (2021)
Abstract: "Adapting to the omnipresent gravitational field was a fundamental basis driving the flourishing of terrestrial plants on the Earth. Plants have evolved a remarkable capability that not only allows them to live and develop within the Earth’s gravity field, but it also enables them to use the gravity vector to guide the growth of roots and shoots, in a process known as gravitropism. Triggered by gravistimulation, plant gravitropism is a highly complex, multistep process that requires many organelles and players to function in an intricate coordinated way. Although this process has been studied for several 100 years, much remains unclear, particularly the early events that trigger the relocation of the auxin efflux carrier PIN-FORMED (PIN) proteins, which presumably leads to the asymmetrical redistribution of auxin. In the past decade, the LAZY gene family has been identified as a crucial player that ensures the proper redistribution of auxin and a normal tropic response for both roots and shoots upon gravistimulation. LAZY proteins appear to be participating in the early steps of gravity signaling, as the mutation of LAZY genes consistently leads to altered auxin redistribution in multiple plant species. The identification and characterization of the LAZY gene family have significantly advanced our understanding of plant gravitropism, and opened new frontiers of investigation into the novel molecular details of the early events of gravitropism. Here we review current knowledge of the LAZY gene family and the mechanism modulated by LAZY proteins for controlling both roots and shoots gravitropism. We also discuss the evolutionary significance and conservation of the LAZY gene family in plants."
Authors: Han-Qing Wang, Wei Xuan, Xin-Yuan Huang, Chuanzao Mao and Fang-Jie Zhao.
Plant and Cell Physiology (2020)
Abstract: "Cadmium (Cd) strongly inhibits root growth, especially the formation of lateral roots (LRs). The mechanism of Cd inhibition on LR formation in rice (Oryza sativa) remains unclear. In this study, we found that LR emergence in rice was inhibited significantly by 1 µM Cd and almost completely arrested by 5 µM Cd. Cadmium suppressed both the formation and subsequent development of the lateral root primordium (LRP). By using transgenic rice expressing the auxin response reporters DR5::GUS and DR5rev::VENUS, we found that Cd markedly reduced the auxin levels in the stele and LRP. Cadmium rapidly downregulated the expression of the auxin efflux transporter genes OsPIN1b, OsPIN1c and OsPIN9 in the stele and LPR. The emergence of LRs in a rice cultivar with a null allele of OsHMA3 (Heavy Metal ATPase 3) was more sensitive to Cd than cultivars with functional alleles. Overexpression of functional OsHMA3 in rice greatly alleviated the inhibitory effect of Cd, but the protective effect of OsHMA3 was abolished by the auxin polar transport inhibitor 1-N-naphthylphthalamic acid. The results suggest that Cd inhibits LR development in rice by disrupting OsPIN-mediated auxin distribution to LPR and OsHMA3 protects against Cd toxicity by sequestering Cd into the vacuoles."
Authors: C. Mesejo, A. Marzal, A. Martínez-Fuentes, C. Reig and M. Agustí.
Scientia Horticulturae (2021)
Highlights: • Citrus mature fruit abscission parallels ACS1 and CitIDA3 upregulation and PIN1-like downregulation. • Abscission sensitive ‘navel-type’ orange produces ethylene whereas abscission resistant ‘Valencia-type’ orange does not. • Auxin reduces abscission upregulating PIN1 and downregulating CitIDA3, but without modifying ethylene production.
Abstract: "While the ethylene-auxin interactions are well documented in model dicots such as tomato (climacteric fruit) during mature fruit abscission, the process is not clearly understood in citrus (non-climacteric fruit). The mature fruit produces very little ethylene but is sensitive to ethylene treatments to induce abscission. By contrast, auxin treatments delay fruit abscission, but the particular role of auxin in the process is unknown. Since the IDA-HAE/HSL2 ethylene-independent pathway seem to regulate organ abscission in both model and crop species, we proposed that auxin treatment delays citrus fruit abscission by reactivating the basipetal auxin flux and reducing CitIDA3 expression, without modifying ethylene synthesis. Comparing orange (C. sinensis) genotypes which differ in their abscission rate, ‘Navelate’ vs. ‘Valencia Late’, we found that the force needed to detach the fruit from the tree (FDF) declines in parallel with 1) an increase of ethylene synthesis and CitIDA3 gene expression, and 2) a reduction of PIN1-like (auxin transporter) gene expresion. Further, auxin (2,4-D) treatment maintains a higher force in the abscission zone upregulating PIN1-like and AUX1-like (auxin transporter) gene expression, and downregulating CitIDA3 gene expression, but without modifying ethylene production. We conclude that the 2,4-D treatment delays citrus mature fruit abscission through an ethylene-independent pathway."
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