ABLs and TMKs are co-receptors for extracellular auxin.

Extracellular perception of auxin, an essential phytohormone in plants, has been debated for decades. Auxin-binding protein 1 (ABP1) physically interacts with quintessential transmembrane kinases (TMKs) and was proposed to act as an extracellular auxin receptor, but its role was disputed because abp1 knockout mutants lack obvious morphological phenotypes. Here, we identified two new auxin-binding proteins, ABL1 and ABL2, that are localized to the apoplast and directly interact with the extracellular domain of TMKs in an auxin-dependent manner. Furthermore, functionally redundant ABL1 and ABL2 genetically interact with TMKs and exhibit functions that overlap with those of ABP1 as well as being independent of ABP1. Importantly, the extracellular domain of TMK1 itself binds auxin and synergizes with either ABP1 or ABL1 in auxin binding. Thus, our findings discovered auxin receptors ABL1 and ABL2 having functions overlapping with but distinct from ABP1 and acting together with TMKs as co-receptors for extracellular auxin.

Beating the break-even point with a discrete-variable-encoded logical qubit.

Quantum error correction (QEC) aims to protect logical qubits from noises by using the redundancy of a large Hilbert space, which allows errors to be detected and corrected in real time1. In most QEC codes2-8, a logical qubit is encoded in some discrete variables, for example photon numbers, so that the encoded quantum information can be unambiguously extracted after processing. Over the past decade, repetitive QEC has been demonstrated with various discrete-variable-encoded scenarios9-17. However, extending the lifetimes of thus-encoded logical qubits beyond the best available physical qubit still remains elusive, which represents a break-even point for judging the practical usefulness of QEC. Here we demonstrate a QEC procedure in a circuit quantum electrodynamics architecture18, where the logical qubit is binomially encoded in photon-number states of a microwave cavity8, dispersively coupled to an auxiliary superconducting qubit. By applying a pulse featuring a tailored frequency comb to the auxiliary qubit, we can repetitively extract the error syndrome with high fidelity and perform error correction with feedback control accordingly, thereby exceeding the break-even point by about 16% lifetime enhancement. Our work illustrates the potential of hardware-efficient discrete-variable encodings for fault-tolerant quantum computation19.

TMK-based cell-surface auxin signalling activates cell-wall acidification.

The phytohormone auxin controls many processes in plants, at least in part through its regulation of cell expansion1. The acid growth hypothesis has been proposed to explain auxin-stimulated cell expansion for five decades, but the mechanism that underlies auxin-induced cell-wall acidification is poorly characterized. Auxin induces the phosphorylation and activation of the plasma membrane H+-ATPase that pumps protons into the apoplast2, yet how auxin activates its phosphorylation remains unclear. Here we show that the transmembrane kinase (TMK) auxin-signalling proteins interact with plasma membrane H+-ATPases, inducing their phosphorylation, and thereby promoting cell-wall acidification and hypocotyl cell elongation in Arabidopsis. Auxin induced interactions between TMKs and H+-ATPases in the plasma membrane within seconds, as well as TMK-dependent phosphorylation of the penultimate threonine residue on the H+-ATPases. Our genetic, biochemical and molecular evidence demonstrates that TMKs directly phosphorylate plasma membrane H+-ATPase and are required for auxin-induced H+-ATPase activation, apoplastic acidification and cell expansion. Thus, our findings reveal a crucial connection between auxin and plasma membrane H+-ATPase activation in regulating apoplastic pH changes and cell expansion through TMK-based cell surface auxin signalling.

PLEIOTROPIC REGULATORY LOCUS1 maintains actin microfilament integrity to regulate pavement cell morphogenesis.

Actin dynamics are critical for plant cell morphogenesis, but the underlying signaling mechanisms regulating these dynamics are not well understood. Here, we established that PLEIOTROPIC REGULATORY LOCUS1 (PRL1) modulates leaf pavement cell (PC) morphogenesis in Arabidopsis (Arabidopsis thaliana) by maintaining the dynamic homeostasis of actin microfilaments (MF). Our previous studies indicated that PC shape was determined by antagonistic RHO-RELATED GTPase FROM PLANTS 2 (ROP2) and RHO-RELATED GTPase FROM PLANTS 6 (ROP6) signaling pathways that promote cortical MF and microtubule organization, respectively. Our genetic screen for additional components in ROP6-mediated signaling identified prl1 alleles. Genetic analysis confirmed that PRL1 plays a key role in PC morphogenesis. Mutations in PRL1 caused cortical MF depolymerization, resulting in defective PC morphogenesis. Further genetic analysis revealed that PRL1 is epistatic to ROP2 and ROP6 in PC morphogenesis. Mutations in PRL1 enhanced the effects of ROP2 and ROP6 in PC morphogenesis, leading to a synergistic phenotype in the PCs of ROP2 prl1 and ROP6 prl1. Furthermore, the activities of ROP2 and ROP6 were differentially altered in prl1 mutants, suggesting that ROP2 and ROP6 function downstream of PRL1. Additionally, cortical MF depolymerization in prl1 mutants occurred independently of ROP2 and ROP6, implying that these proteins impact PC morphogenesis in the prl1 mutant through other cellular processes. Our research indicates that PRL1 preserves the structural integrity of actin and facilitates pavement cell morphogenesis in Arabidopsis.

Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis.

Auxin is a multifunctional hormone essential for plant development and pattern formation. A nuclear auxin-signaling system controlling auxin-induced gene expression is well established, but cytoplasmic auxin signaling, as in its coordination of cell polarization, is unexplored. We found a cytoplasmic auxin-signaling mechanism that modulates the interdigitated growth of Arabidopsis leaf epidermal pavement cells (PCs), which develop interdigitated lobes and indentations to form a puzzle-piece shape in a two-dimensional plane. PC interdigitation is compromised in leaves deficient in either auxin biosynthesis or its export mediated by PINFORMED 1 localized at the lobe tip. Auxin coordinately activates two Rho GTPases, ROP2 and ROP6, which promote the formation of complementary lobes and indentations, respectively. Activation of these ROPs by auxin occurs within 30 s and depends on AUXIN-BINDING PROTEIN 1. These findings reveal Rho GTPase-based auxin-signaling mechanisms, which modulate the spatial coordination of cell expansion across a field of cells.

ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis.

Spatial distribution of the plant hormone auxin regulates multiple aspects of plant development. These self-regulating auxin gradients are established by the action of PIN auxin transporters, whose activity is regulated by their constitutive cycling between the plasma membrane and endosomes. Here, we show that auxin signaling by the auxin receptor AUXIN-BINDING PROTEIN 1 (ABP1) inhibits the clathrin-mediated internalization of PIN proteins. ABP1 acts as a positive factor in clathrin recruitment to the plasma membrane, thereby promoting endocytosis. Auxin binding to ABP1 interferes with this action and leads to the inhibition of clathrin-mediated endocytosis. Our study demonstrates that ABP1 mediates a nontranscriptional auxin signaling that regulates the evolutionarily conserved process of clathrin-mediated endocytosis and suggests that this signaling may be essential for the developmentally important feedback of auxin on its own transport.

Arabidopsis AAR2, a conserved splicing factor in eukaryotes, acts in microRNA biogenesis.

MicroRNAs (miRNAs) play an essential role in plant growth and development, and as such, their biogenesis is fine-tuned via regulation of the core microprocessor components. Here, we report that Arabidopsis AAR2, a homolog of a U5 snRNP assembly factor in yeast and humans, not only acts in splicing but also promotes miRNA biogenesis. AAR2 interacts with the microprocessor component hyponastic leaves 1 (HYL1) in the cytoplasm, nucleus, and dicing bodies. In aar2 mutants, abundance of nonphosphorylated HYL1, the active form of HYL1, and the number of HYL1-labeled dicing bodies are reduced. Primary miRNA (pri-miRNA) accumulation is compromised despite normal promoter activities of MIR genes in aar2 mutants. RNA decay assays show that the aar2-1 mutation leads to faster degradation of pri-miRNAs in a HYL1-dependent manner, which reveals a previously unknown and negative role of HYL1 in miRNA biogenesis. Taken together, our findings reveal a dual role of AAR2 in miRNA biogenesis and pre-messenger RNA splicing.

Membrane nanodomains: Dynamic nanobuilding blocks of polarized cell growth.

Cell polarity is intimately linked to numerous biological processes, such as oriented plant cell division, particular asymmetric division, cell differentiation, cell and tissue morphogenesis, and transport of hormones and nutrients. Cell polarity is typically initiated by a polarizing cue that regulates the spatiotemporal dynamic of polarity molecules, leading to the establishment and maintenance of polar domains at the plasma membrane. Despite considerable progress in identifying key polarity regulators in plants, the molecular and cellular mechanisms underlying cell polarity formation have yet to be fully elucidated. Recent work suggests a critical role for membrane protein/lipid nanodomains in polarized morphogenesis in plants. One outstanding question is how the spatiotemporal dynamics of signaling nanodomains are controlled to achieve robust cell polarization. In this review, we first summarize the current state of knowledge on potential regulatory mechanisms of nanodomain dynamics, with a special focus on Rho-like GTPases from plants. We then discuss the pavement cell system as an example of how cells may integrate multiple signals and nanodomain-involved feedback mechanisms to achieve robust polarity. A mechanistic understanding of nanodomains' roles in plant cell polarity is still in the early stages and will remain an exciting area for future investigations.

The long noncoding RNA FRILAIR regulates strawberry fruit ripening by functioning as a noncanonical target mimic.

Long noncoding RNAs (lncRNAs) are emerging as important regulators in plant development, but few of them have been functionally characterized in fruit ripening. Here, we have identified 25,613 lncRNAs from strawberry ripening fruits based on RNA-seq data from poly(A)-depleted libraries and rRNA-depleted libraries, most of which exhibited distinct temporal expression patterns. A novel lncRNA, FRILAIR harbours the miR397 binding site that is highly conserved in diverse strawberry species. FRILAIR overexpression promoted fruit maturation in the Falandi strawberry, which was consistent with the finding from knocking down miR397, which can guide the mRNA cleavage of both FRILAIR and LAC11a (encoding a putative laccase-11-like protein). Moreover, LAC11a mRNA levels were increased in both FRILAIR overexpressing and miR397 knockdown fruits, and accelerated fruit maturation was also found in LAC11a overexpressing fruits. Overall, our study demonstrates that FRILAIR can act as a noncanonical target mimic of miR397 to modulate the expression of LAC11a in the strawberry fruit ripening process.

Extranuclear auxin signaling: a new insight into auxin's versatility.

Auxin phytohormone has a role in most aspects of the life of a land plant and is found even in ancient plants such as single-cell green algae. Auxin's ubiquitous but specific effects have been mainly explained by the extraordinary ability of plants to interpret spatiotemporal patterns of auxin concentrations via the regulation of gene transcription. This is thought to be achieved through the combinatorial effects of two families of nuclear coreceptor proteins, that is the TRANSPORT INHIBITOR RESPONSE1 and AUXIN-SIGNALING F-BOX (TIR1/AFB) and AUXIN/INDOLE ACETIC ACID. Recent evidence has suggested transcription-independent roles of TIR1/AFBs localized outside the nucleus and TRANSMEMBRANE KINASE (TMK)-based auxin signaling occurring in the plasma membrane. Furthermore, emerging evidence supports a coordinated action of the intra- and extranuclear auxin signaling pathways to regulate specific auxin responses. Here, we highlight how auxin signaling acts inside and outside the nucleus for the regulation of growth and morphogenesis and propose that the future direction of auxin biology lies in the elucidation of a new collaborative paradigm of intra- and extranuclear auxin signaling.

CamelliA-based simultaneous imaging of Ca2+ dynamics in subcellular compartments.

As a universal second messenger, calcium (Ca2+) transmits specific cellular signals via a spatiotemporal signature generated from its extracellular source and internal stores. Our knowledge of the mechanisms underlying the generation of a Ca2+ signature is hampered by limited tools for simultaneously monitoring dynamic Ca2+ levels in multiple subcellular compartments. To overcome the limitation and to further improve spatiotemporal resolutions, we have assembled a molecular toolset (CamelliA lines) in Arabidopsis (Arabidopsis thaliana) that enables simultaneous and high-resolution monitoring of Ca2+ dynamics in multiple subcellular compartments through imaging different single-colored genetically encoded calcium indicators. We uncovered several Ca2+ signatures in three types of Arabidopsis cells in response to internal and external cues, including rapid oscillations of cytosolic Ca2+ and apical plasma membrane Ca2+ influx in fast-growing Arabidopsis pollen tubes, the spatiotemporal relationship of Ca2+ dynamics in four subcellular compartments of root epidermal cells challenged with salt, and a shockwave-like Ca2+ wave propagating in laser-wounded leaf epidermis. These observations serve as a testimony to the wide applicability of the CamelliA lines for elucidating the subcellular sources contributing to the Ca2+ signatures in plants.

Effective protocol for generating NOON states of resonator modes.

We propose a protocol for the generation of NOON states of resonator modes. The physical model is composed of two Kerr-nonlinear resonators and a four-level qudit. Using the off-resonant couplings between the resonators and the qudit, qudit-level-dependent frequency shifts on the two resonators are induced. The frequency shifts allow us to drive different resonators to the N-photon state when the qudit is in different intermediate levels. Consequently, the generation of NOON states with arbitrary photon number N can be completed in only three steps, i.e., driving the qudit to a superposition state of the two intermediate levels, driving one of the resonators to its N-photon state, and driving the qudit back to its ground level. Numerical simulations show that, in the regime of strong Kerr nonlinearity and coupling strengths, the protocol can produce the NOON state with high fidelity in the cases of different photon numbers. In addition, it is possible for the protocol to produce acceptable fidelity in the presence of systematic errors and decoherence factors. Therefore, the protocol may provide some useful perspectives for effective generation of photonic NOON states.

Quantum metric and metrology with parametrically-driven Tavis-Cummings models.

We study the quantum metric in a driven Tavis-Cummings model, comprised of multiple qubits interacting with a quantized photonic field. The parametrical driving of the photonic field breaks the system's U(1) symmetry down to a Z2 symmetry, whose spontaneous breaking initiates a superradiant phase transition. We analytically solved the eigenenergies and eigenstates, and numerically simulated the system behaviors near the critical point. The critical behaviors near the superradiant phase transition are characterized by the quantum metric, defined in terms of the response of the quantum state to variation of the control parameter. In addition, a quantum metrological protocol based on the critical behaviors of the quantum metric near the superradiant phase transition is proposed, which enables greatly the achievable measurement precision.

Exceptional Entanglement Phenomena: Non-Hermiticity Meeting Nonclassicality.

Non-Hermitian (NH) extension of quantum-mechanical Hamiltonians represents one of the most significant advancements in physics. During the past two decades, numerous captivating NH phenomena have been revealed and demonstrated, but all of which can appear in both quantum and classical systems. This leads to the fundamental question: what NH signature presents a radical departure from classical physics? The solution of this problem is indispensable for exploring genuine NH quantum mechanics, but remains experimentally untouched so far. Here, we resolve this basic issue by unveiling distinct exceptional entanglement phenomena, exemplified by an entanglement transition, occurring at the exceptional point of NH interacting quantum systems. We illustrate and demonstrate such purely quantum-mechanical NH effects with a naturally dissipative light-matter system, engineered in a circuit quantum electrodynamics architecture. Our results lay the foundation for studies of genuinely quantum-mechanical NH physics, signified by exceptional-point-enabled entanglement behaviors.

Observation of a Superradiant Phase Transition with Emergent Cat States.

Superradiant phase transitions (SPTs) are important for understanding light-matter interactions at the quantum level, and play a central role in criticality-enhanced quantum sensing. So far, SPTs have been observed in driven-dissipative systems, but the emergent light fields did not show any nonclassical characteristic due to the presence of strong dissipation. Here we report an experimental demonstration of the SPT featuring the emergence of a highly nonclassical photonic field, realized with a resonator coupled to a superconducting qubit, implementing the quantum Rabi model. We fully characterize the light-matter state by Wigner matrix tomography. The measured matrix elements exhibit quantum interference intrinsic of a photonic mesoscopic superposition, and reveal light-matter entanglement.

Determination of volatile profiles of woodland strawberry (Fragaria vesca) during fruit maturation by HS-SPME GC-MS.

BACKGROUND: Aroma is an important agronomic trait for strawberries, and the improvement of fruit flavor is a key goal in current strawberry breeding programs. Fragaria vesca (also known as woodland strawberry) has become an excellent model plant with exquisite flavor, a small genome size and a short life cycle. Thus, the comprehensive identification of fruit volatiles and their accumulation pattern of F. vesca strawberries are very important and necessary to the fruit aroma study. This study examined the volatile profile changes from the fruits of three F. vesca genotypes during maturation using headspace solid-phase microextraction combined with gas chromatography-mass spectrometry with multivariate analysis. RESULTS: A total of 191 putative volatile compounds were identified, while 152, 159 and 175 volatiles were detected in 20-30 DAP (days after pollination) fruits of Hawaii 4 (HW), Reugen (RG) and Yellow Wonder (YW), respectively. Aldehydes and alcohols predominated in the early time point while esters were predominant during the late time point. Ketones were the dominant compounds from F. vesca strawberries at the ripe stage. Certain genotype-characteristic volatiles were identified, including eugenol, γ-octalactone and δ-decalactone only detected in YW, and mesifurane was found in HW. CONCLUSIONS: RG and YW showed very similar volatile compositions, but YW presented a greater number of volatiles and RG yielded a higher content. Differences in the volatile composition may be primarily due to genetic relationships. The metabolic changes that occurred during fruit ripening and characteristic volatiles will be a useful reference for future studies of strawberry volatiles. © 2023 Society of Chemical Industry.

The Rho-family GTPase OsRac1 controls rice grain size and yield by regulating cell division.

Grain size is a key factor for determining grain yield in crops and is a target trait for both domestication and breeding, yet the mechanisms underlying the regulation of grain size are largely unclear. Here we show that the grain size and yield of rice (Oryza sativa) is positively regulated by ROP GTPase (Rho-like GTPase from plants), a versatile molecular switch modulating plant growth, development, and responses to the environment. Overexpression of rice OsRac1ROP not only increases cell numbers, resulting in a larger spikelet hull, but also accelerates grain filling rate, causing greater grain width and weight. As a result, OsRac1 overexpression improves grain yield in O. sativa by nearly 16%. In contrast, down-regulation or deletion of OsRac1 causes the opposite effects. RNA-seq and cell cycle analyses suggest that OsRac1 promotes cell division. Interestingly, OsRac1 interacts with and regulates the phosphorylation level of OsMAPK6, which is known to regulate cell division and grain size in rice. Thus, our findings suggest OsRac1 modulates rice grain size and yield by influencing cell division. This study provides insights into the molecular mechanisms underlying the control of rice grain size and suggests that OsRac1 could serve as a potential target gene for breeding high-yield crops.

Arabinogalactan protein-rare earth element complexes activate plant endocytosis.

Endocytosis is essential to all eukaryotes, but how cargoes are selected for internalization remains poorly characterized. Extracellular cargoes are thought to be selected by transmembrane receptors that bind intracellular adaptors proteins to initiate endocytosis. Here, we report a mechanism for clathrin-mediated endocytosis (CME) of extracellular lanthanum [La(III)] cargoes, which requires extracellular arabinogalactan proteins (AGPs) that are anchored on the outer face of the plasma membrane. AGPs were colocalized with La(III) on the cell surface and in La(III)-induced endocytic vesicles in Arabidopsis leaf cells. Superresolution imaging showed that La(III) triggered AGP movement across the plasma membrane. AGPs were then colocalized and physically associated with the µ subunit of the intracellular adaptor protein 2 (AP2) complexes. The AGP-AP2 interaction was independent of CME, whereas AGP's internalization required CME and AP2. Moreover, we show that AGP-dependent endocytosis in the presence of La(III) also occurred in human cells. These findings indicate that extracellular AGPs act as conserved CME cargo receptors, thus challenging the current paradigm about endocytosis of extracellular cargoes.

GTPase ROP2 binds and promotes activation of target of rapamycin, TOR, in response to auxin.

Target of rapamycin (TOR) promotes reinitiation at upstream ORFs (uORFs) in genes that play important roles in stem cell regulation and organogenesis in plants. Here, we report that the small GTPase ROP2, if activated by the phytohormone auxin, promotes activation of TOR, and thus translation reinitiation of uORF-containing mRNAs. Plants with high levels of active ROP2, including those expressing constitutively active ROP2 (CA-ROP2), contain high levels of active TOR ROP2 physically interacts with and, when GTP-bound, activates TOR in vitro TOR activation in response to auxin is abolished in ROP-deficient rop2 rop6 ROP4 RNAi plants. GFP-TOR can associate with endosome-like structures in ROP2-overexpressing plants, indicating that endosomes mediate ROP2 effects on TOR activation. CA-ROP2 is efficient in loading uORF-containing mRNAs onto polysomes and stimulates translation in protoplasts, and both processes are sensitive to TOR inhibitor AZD-8055. TOR inactivation abolishes ROP2 regulation of translation reinitiation, but not its effects on cytoskeleton or intracellular trafficking. These findings imply a mode of translation control whereby, as an upstream effector of TOR, ROP2 coordinates TOR function in translation reinitiation pathways in response to auxin.

Glycolysis regulates pollen tube polarity via Rho GTPase signaling.

As a universal energy generation pathway utilizing carbon metabolism, glycolysis plays an important housekeeping role in all organisms. Pollen tubes expand rapidly via a mechanism of polarized growth, known as tip growth, to deliver sperm for fertilization. Here, we report a novel and surprising role of glycolysis in the regulation of growth polarity in Arabidopsis pollen tubes via impingement of Rho GTPase-dependent signaling. We identified a cytosolic phosphoglycerate kinase (pgkc-1) mutant with accelerated pollen germination and compromised pollen tube growth polarity. pgkc-1 mutation greatly diminished apical exocytic vesicular distribution of REN1 RopGAP (Rop GTPase activating protein), leading to ROP1 hyper-activation at the apical plasma membrane. Consequently, pgkc-1 pollen tubes contained higher amounts of exocytic vesicles and actin microfilaments in the apical region, and showed reduced sensitivity to Brefeldin A and Latrunculin B, respectively. While inhibition of mitochondrial respiration could not explain the pgkc-1 phenotype, the glycolytic activity is indeed required for PGKc function in pollen tubes. Moreover, the pgkc-1 pollen tube phenotype was mimicked by the inhibition of another glycolytic enzyme. These findings highlight an unconventional regulatory function for a housekeeping metabolic pathway in the spatial control of a fundamental cellular process.