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Authors: HuiFang Xu and Xu Chen.
Scientia Sinica Vitae (2024)
Abstract: "Auxin is widely involved in plant growth and development and its adaptation to the environment, and is the most important hormone in plants. In the past two decades, studies based on the model plant Arabidopsis thaliana have confirmed that establishment of auxin gradient through biosynthesis, metabolism, polar transport and signaling pathways determines organogenesis and polarity of plant organs. With the development of gene editing and molecular breeding research, how to apply the theoretical results related to auxin pathway in crop improvement, and coordinate the ideal plant/root type of crops through the selection and combination of dominant genes is a key issue in this field. In this review, we summarize the latest research progress in auxin field in the past five years, refer to the contribution of auxin to the improvement of rice agronomic traits, and discuss and look forward to the possibility of auxin application on soybean breeding."
Authors: Maria Florencia Ercoli, Alexandra Shigenaga, Artur Teixeira de Araujo Junior, Rashmi Jain and Pamela Ronald.
bioRxiv (2024)
Abstract: "In Arabidopsis roots, growth initiation and cessation are organized into distinct zones. How regulatory mechanisms are integrated to coordinate these processes and maintain proper growth progression over time is not well understood. Here, we demonstrate that the peptide hormone PLANT PEPTIDE CONTAINING SULFATED TYROSINE 1 (PSY1) promotes root growth by controlling cell elongation. Higher levels of PSY1 lead to longer differentiated cells with a shootward displacement of characteristics common to mature cells. PSY1 activates genes involved in the biosynthesis of flavonols, a group of plant-specific secondary metabolites. Using genetic and chemical approaches, we show that flavonols are required for PSY1 function. Flavonol accumulation downstream of PSY1 occurs in the differentiation zone, where PSY1 also reduces auxin and reactive oxygen species (ROS) activity. These findings support a model where PSY1 signals the developmental-specific accumulation of secondary metabolites to regulate the extent of cell elongation and the overall progression to maturation."
Authors: Adrián González Ortega-Villaizán, Eoghan King, Manish K. Patel, Marta-Marina Pérez- Alonso, Sandra S. Scholz, Hitoshi Sakakibara, Takatoshi Kiba, Mikiko Kojima, Yumiko Takebayashi, Patricio Ramos, Luis Morales-Quintana, Sarah Breitenbach, Ana Smolko, Branka Salopek-Sondi, Nataša Bauer, Jutta Ludwig-Müller, Anne Krapp, Ralf Oelmüller, Jesús Vicente-Carbajosa and Stephan Pollmann.
bioRxiv (2024)
Abstract: "Plants share their habitats with a multitude of different microbes. This close vicinity promoted the evolution of inter-organismic interactions between plants and many different microorganisms that provide mutual growth benefits both to the plant and the microbial partner. The symbiosis of Arabidopsis thaliana with the beneficial root colonizing endophyte Serendipita indica represents a well-studied system. Co-colonization of Arabidopsis roots with S. indica significantly promotes plant growth. Due to the notable phenotypic alterations of fungus-infected root systems, the involvement of a reprogramming of plant hormone levels, especially that of indole-3-acetic acid, has been suggested earlier. However, until now, the molecular mechanism by which S. indica promotes plant growth remains largely unknown. This study used comprehensive transcriptomics, metabolomics, reverse genetics, and life cell imaging to reveal the intricacies of auxin-related processes that affect root growth in the symbiosis between A. thaliana and S. indica. Our experiments revealed the essential role of tightly controlled auxin conjugation in the plant-fungus interaction. It particularly highlighted the importance of two GRETCHEN HAGEN 3 (GH3) genes, GH3.5 and GH3.17, for the fungus infection-triggered stimulation of biomass production, thus broadening our knowledge about the function of GH3s in plants. Furthermore, we provide evidence for the transcriptional alteration of the PIN2 auxin transporter gene in roots of Arabidopsis seedlings infected with S. indica and demonstrate that this transcriptional adjustment affects auxin signaling in roots, which results in increased plant growth."
Authors: Ulrich Z. Hammes and Bjørn Panyella Pedersen.
Annual Review of Plant Biology (2024)
Abstract: "Auxins, a group of central hormones in plant growth and development, are transported by a diverse range of transporters with distinct biochemical and structural properties. This review summarizes the current knowledge on all known auxin transporters with respect to their biochemical and biophysical properties and the methods used to characterize them. In particular, we focus on the recent advances that were made concerning the PIN-FORMED family of auxin exporters. Insights derived from solving their structures have improved our understanding of the auxin export process, and we discuss the current state of the art on PIN-mediated auxin transport, including the use of biophysical methods to examine their properties. Understanding the mechanisms of auxin transport is crucial for understanding plant growth and development, as well as for the development of more effective strategies for crop production and plant biotechnology."
Authors: Sophie Farkas and Jürgen Kleine-Vehn.
Current Biology (2023)
Summary: Plant gravitropism has fascinated scientists for centuries. A new study provides a major mechanistic update of the so-called starch/statolith hypothesis, revealing how gravity perception is converted into a physiological response.
Excerpts: "The gravitational force serves as a stable reference for plant growth. This information allows plants to orient their shoots and roots vertically, even in the absence of other environmental cues like light. To achieve this, plants must sense gravity and translate this physical stimulus into a physiological response. In a new study, Chen and colleagues1 have now molecularly described the conversion mechanism, allowing plants to relate their growth to gravity."
"Intriguingly, two recent publications1,11 revealed that LZY proteins not only localize to the plasma membrane, but also to the surface of the amyloplasts. Chen and colleagues1 clearly illustrate that LZY proteins sediment together with the amyloplast downwards, where the LZY proteins will subsequently translocate to the plasma membrane of the new bottom side. Accordingly, this intracellular ‘hitchhiking’ mechanism allows the gravity-induced polarization of LZY, ultimately pinpointing the redirection of auxin flow."
"This study provides a molecular explanation for the conversion of a physical signal into a physiological response during gravitropism1. It unveils an intriguing intracellular hitchhiking mechanism that connects amyloplast sedimentation with the asymmetric delivery of LZY proteins to the new lower side of the cell. A central player in this mechanism is the MPK3–MKK5 cascade, which phosphorylates LZY proteins upon gravistimulation, enhancing their interaction with TOC proteins at the amyloplast (Figure 1)."
Authors: Marta Del Bianco, Jiří Friml, Lucia Strader and Stefan Kepinski.
Journal of Experimental Botany (2023)
Abstract: "Amid the delays due to the global pandemic, in early October 2022, the auxin community gathered in the idyllic peninsula of Cavtat, Croatia. More than 170 scientists from across the world converged to discuss the latest advancements in fundamental and applied research in the field. The topics, from signalling and transport to plant architecture and response to the environment, show how auxin research must bridge from the molecular realm to macroscopic developmental responses. This is mirrored in this collection of reviews, contributed by participants of the Auxin 2022 meeting."
Authors: Xin Song, Yaoguang Yu, Jiameng Zhu and Chenlong Li.
Planta (2024)
Main conclusion: This study reveals that mutations in BRIP1/2 subunits of the BAS complex disrupt root meristem development by decreasing PIN genes expression, affecting auxin transport, and downregulating essential root genes PLT.
Abstract: "Abstract Switch defective/sucrose non-fermentable (SWI/SNF) chromatin remodeling complexes play vital roles in plant development. BRAHMA-interacting proteins1 (BRIP1) and BRIP2 are subunits of BRAHMA (BRM)-associated SWI/SNF complex (BAS) in plants; however, their role and underlying regulatory mechanism in root development are still unknown. Here, we show that brip1 brip2 double mutants have a significantly shortened root meristem and an irregular arrangement in a portion of the root stem cell niche. The mutations in BRIP1 and BRIP2 cause decreased expression of the PIN-FORMED (PIN) genes, which in turn reduces the transport of auxin at the root tip, leading to the disruption of the accurate establishment of normal auxin concentration gradients in the stem cells. Chromatin immunoprecipitation (ChIP) experiments indicated that BRIP1 and BRIP2 directly bind to the PINs. Furthermore, we found a significant down-regulation in the expression of key root development genes, PLETHORA (PLT), in brip1 brip2. The brip1 brip2 plt1 plt2 quadruple mutations do not show further exacerbation in the short-root phenotype compared to plt1 plt2 double mutants. Using a dexamethasone (DEX)-inducible PLT2 transgenic line, we showed that acute overexpression of PLT2 partially rescues root meristem defects of brip1 brip2, suggesting that BRIP1 and BRIP2 act in part through the PLT1/2 pathway. Taken together, our results identify the critical role and the underlying mechanism of BRIP1/2 in maintaining the development of root meristem through the regulation of auxin output and expression of PLTs."
Authors: Shuping Jiao, Sujan Mamidi, Mark A. Chamberlin, Mary Beatty, Shawn Thatcher, Kevin D. Simcox, Fanna Maina, Hu Wang-Nan, Gurmukh S. Johal, Lynn Heetland, Sandeep R. Marla, Robert B. Meeley, Jeremy Schmutz, Geoffrey P. Morris and Dilbag S. Multani.
New Phytologist (2023)
Abstract: "In the current genomic era, the search and deployment of new semi-dwarf alleles have continued to develop better plant types in all cereals. We characterized an agronomically optimal semi-dwarf mutation in Zea mays L. and a parallel polymorphism in Sorghum bicolor L. We cloned the maize brachytic1 (br1-Mu) allele by a modified PCR-based Sequence Amplified Insertion Flanking Fragment (SAIFF) approach. Histology and RNA-Seq elucidated the mechanism of semi-dwarfism. GWAS linked a sorghum plant height QTL with the Br1 homolog by resequencing a West African sorghum landraces panel. The semi-dwarf br1-Mu allele encodes an MYB transcription factor78 that positively regulates stalk cell elongation by interacting with the polar auxin pathway. Semi-dwarfism is due to differential splicing and low functional Br1 wild-type transcript expression. The sorghum ortholog, SbBr1, co-segregates with the major plant height QTL qHT7.1 and is alternatively spliced. The high frequency of the Sbbr1 allele in African landraces suggests that African smallholder farmers used the semi-dwarf allele to improve plant height in sorghum long before efforts to introduce Green Revolution-style varieties in the 1960s. Surprisingly, variants for differential splicing of Brachytic1 were found in both commercial maize and smallholder sorghum, suggesting parallel tuning of plant architecture across these systems."
Authors: Ning Zhang, Songtao Gui and Yonghong Wang.
Molecular Plant (2023)
Excerpts: "Recently, two separate research groups have made noteworthy contributions to our understanding of gravity sensing in plants by investigating the role of amyloplast sedimentation in repolarizing LAZY/LZY proteins (Chen et al., 2023; Nishimura et al., 2023). Both studies observed the LAZY/LZY localization on the amyloplast and PM, and translocation of LAZY/LZY from statoliths to the PM in response to gravistimulation."
"Furthermore, Nishimura et al. (2023) discovered that AtLAZY/LZY polar localization can rapidly change upon gravistimulation, resulting in repolarization in the new gravity direction. More importantly, they also explicitly demonstrated the essential role of amyloplast sedimentation in achieving the polarization of AtLAZY/LZY on the PM by manipulating the amyloplasts with the optical tweezer. In this study, authors demonstrated AtLAZY/LZY polarity on the PM is established based on the amyloplast position, achieved through AtLAZY/LZY translocation from amyloplast to the PM."
"Chen et al. (2023) proposed a model for gravity perception in plant roots: Gravistimulation increases the phosphorylation of AtLAZY/LZY mediated by MAPK. This phosphorylation, in turn, strengthens the interaction between AtLAZY/LZY and TOCs on the surface of amyloplasts. Subsequently, amyloplast sedimentation takes AtLAZY/LZY to the new bottom of columella cells. Ultimately, AtLAZY/LZY translocates from amyloplasts to the adjacent PM, establishing a new polarity (Figure 1). These findings represent significant progress in our understanding of gravity sensing mechanisms in plants."
Authors: Noel Blanco-Touriñán and Christian S. Hardtke.
Current Opinion in Plant Biology (2023)
Highlights: • Live-cell imaging reveals the cellular basis for cotyledon vein formation. • New polar auxin transport regulatory mechanisms in vein formation were identified. • Polar auxin transport-independent mechanisms emerge as regulators of vein formation. • scRNA-seq suggests transitional stages for lateral root vascular identity acquisition. • Vasculature formation in lateral roots requires coordination of primary root tissues.
Abstract: "The vascular system was essential for plants to colonize land by facilitating the transport of water, nutrients, and minerals throughout the body. Our current knowledge on the molecular-genetic control of vascular tissue specification and differentiation is mostly based on studies in the Arabidopsis primary root. To what degree these regulatory mechanisms in the root meristem can be extrapolated to vascular tissue development in other organs is a question of great interest. In this review, we discuss the most recent progress on cotyledon vein formation, with a focus on polar auxin transport-dependent and -independent mechanisms. We also provide an overview of vasculature formation in postembryonic organs, namely lateral roots, which is more complex than anticipated as several tissues of the parent root must act in a spatio-temporally coordinated manner."
Authors: Mohammed M. Mira, Eman A. El-Khateeb, Mohamed S. Youssef, Katarzyna Ciacka, Kenny So, Robert W. Duncan, Robert D. Hill and Claudio Stasolla.
Planta (2023)
Main conclusion: Over-expression of phytoglobin mitigates the degradation of the root apical meristem (RAM) caused by waterlogging through changes in nitric oxide and auxin distribution at the root tip.
Abstract: "Plant performance to waterlogging is ameliorated by the over-expression of the Arabidopsis Phytoglobin 1 (Pgb1) which also contributes to the maintenance of a functional RAM. Hypoxia induces accumulation of ROS and damage in roots of wild type plants; these events were preceded by the exhaustion of the RAM resulting from the loss of functionality of the WOX5-expressing quiescent cells (QCs). These phenotypic deviations were exacerbated by suppression of Pgb1 and attenuated when the same gene was up-regulated. Genetic and pharmacological studies demonstrated that degradation of the RAM in hypoxic roots is attributed to a reduction in the auxin maximum at the root tip, necessary for the specification of the QC. This reduction was primarily caused by alterations in PIN-mediated auxin flow but not auxin synthesis. The expression and localization patterns of several PINs, including PIN1, 2, 3 and 4, facilitating the basipetal translocation of auxin and its distribution at the root tip, were altered in hypoxic WT and Pgb1-suppressing roots but mostly unchanged in those over-expressing Pgb1. Disruption of PIN1 and PIN2 signal in hypoxic roots suppressing Pgb1 initiated in the transition zone at 12 h and was specifically associated to the absence of Pgb1 protein in the same region. Exogenous auxin restored a functional RAM, while inhibition of the directional auxin flow exacerbated the degradation of the RAM. The regulation of root behavior by Pgb1 was mediated by nitric oxide (NO) in a model consistent with the recognized function of Pgbs as NO scavengers. Collectively, this study contributes to our understanding of the role of Pgbs in preserving root meristem function and QC niche during conditions of stress, and suggests that the root transition zone is most vulnerable to hypoxia.
Authors: Carlos Hernán Barrera-Rojas, Mateus Henrique Vicente, Diego Armando Pinheiro Brito, Eder M. Silva, Aitor Muñoz Lopez, Leticia F. Ferigolo, Rafael Monteiro do Carmo, Carolina M. S. Silva, Geraldo F. F. Silva, Joao P. O. Correa, Marcela M. Notini, Luciano Freschi, Pilar Cubas and Fabio T. S. Nogueira.
Journal of Experimental Botany (2023)
Abstract: "The miRNA156 (miR156)/SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL/SBP) regulatory hub is highly conserved among phylogenetically distinct species, but how it interconnects multiple pathways to converge to common integrators controlling shoot architecture is still unclear. Here, we demonstrated that the miR156/SlSBP15 node modulates tomato shoot branching by connecting multiple phytohormones with classical genetic pathways regulating both axillary bud development and outgrowth. miR156-overexpressing plants (156-OE) displayed high shoot branching, whereas plants overexpressing a miR156-resistant SlSBP15 allele (rSBP15) showed arrested shoot branching. Importantly, the rSBP15 allele was able to partially restore the wild-type shoot branching phenotype in the 156-OE background. rSBP15 plants have tiny axillary buds, and their activation is dependent on shoot apex-derived auxin transport inhibition. Hormonal measurements revealed that indole-3-acetic acid (IAA) and abscisic acid (ABA) concentrations were lower in 156-OE and higher in rSBP15 axillary buds, respectively. Genetic and molecular data indicated that SlSBP15 regulates axillary bud development and outgrowth by inhibiting auxin transport and GOBLET (GOB) activity, and by interacting with tomato BRANCHED1b (SlBRC1b) to control ABA levels within axillary buds. Collectively, our data provide a new mechanism by which the miR156/SPL/SBP hub regulates shoot branching, and suggest that modulating SlSBP15 activity might have potential applications in shaping tomato shoot architecture."
Authors: Suruchi Roychoudhry, Katelyn Sageman-Furnas, Chris Wolverton, Peter Grones, Shutang Tan, Gergely Molnár, Martina De Angelis, Heather L. Goodman, Nicola Capstaff, James P. B. Lloyd, Jack Mullen, Roger Hangarter, Jiří Friml and Stefan Kepinski.
Nature Plants (2023)
Editor's view: Lateral roots grow at specific angles with respect to gravity. Two auxin transporters, PIN3 and PIN7, in gravi-sensing cells establish hormone gradients that balance downward and upward growth to generate stable, non-vertical roots.
Abstract: "Lateral roots are typically maintained at non-vertical angles with respect to gravity. These gravitropic setpoint angles are intriguing because their maintenance requires that roots are able to effect growth response both with and against the gravity vector, a phenomenon previously attributed to gravitropism acting against an antigravitropic offset mechanism. Here we show how the components mediating gravitropism in the vertical primary root—PINs and phosphatases acting upon them—are reconfigured in their regulation such that lateral root growth at a range of angles can be maintained. We show that the ability of Arabidopsis lateral roots to bend both downward and upward requires the generation of auxin asymmetries and is driven by angle-dependent variation in downward gravitropic auxin flux acting against angle-independent upward, antigravitropic flux. Further, we demonstrate a symmetry in auxin distribution in lateral roots at gravitropic setpoint angle that can be traced back to a net, balanced polarization of PIN3 and PIN7 auxin transporters in the columella. These auxin fluxes are shifted by altering PIN protein phosphoregulation in the columella, either by introducing PIN3 phosphovariant versions or via manipulation of levels of the phosphatase subunit PP2A/RCN1. Finally, we show that auxin, in addition to driving lateral root directional growth, acts within the lateral root columella to induce more vertical growth by increasing RCN1 levels, causing a downward shift in PIN3 localization, thereby diminishing the magnitude of the upward, antigravitropic auxin flux."
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Authors: Chao Tan, Suxin Li, Jia Song, Xianfu Zheng, Hao Zheng, Weichang Xu, Cui Wan, Tan Zhang, Qiang Bian and Shuzhen Men.
Communications Biology (2024)
Editor's view: Physiological and molecular studies have shown that 3,4-dichlorophenylacetic acid (Dcaa) has auxin-like activity and acts through the auxin signaling pathway in plants. This provides a basis for the application of Dcaa in agricultural practice.
Abstract: "Auxins and their analogs are widely used to promote root growth, flower and fruit development, and yield in crops. The action characteristics and application scope of various auxins are different. To overcome the limitations of existing auxins, expand the scope of applications, and reduce side effects, it is necessary to screen new auxin analogs. Here, we identified 3,4-dichlorophenylacetic acid (Dcaa) as having auxin-like activity and acting through the auxin signaling pathway in plants. At the physiological level, Dcaa promotes the elongation of oat coleoptile segments, the generation of adventitious roots, and the growth of crop roots. At the molecular level, Dcaa induces the expression of auxin-responsive genes and acts through auxin receptors. Molecular docking results showed that Dcaa can bind to auxin receptors, among which TIR1 has the highest binding activity. Application of Dcaa at the root tip of the DR5:GUS auxin-responsive reporter induces GUS expression in the root hair zone, which requires the PIN2 auxin efflux carrier. Dcaa also inhibits the endocytosis of PIN proteins like other auxins. These results provide a basis for the application of Dcaa in agricultural practices."
Authors: Z. Tang, Y. Zhang, Y. Ma, D. Zhao, J. Dong and H. Zhang.
Biologia Plantarum (2024)
Abstract: "Roots are important for plant anchoring, water and nutrient absorption, and other physiological processes. Gravity is a primary determinant of the spatial distribution of plant roots in the soil. Therefore, in-depth understanding of the molecular mechanisms and biochemical networks of root responses to gravity has both theoretical and practical significance in guiding the genetic improvement of plants. Gravitropism, the process through which plants sense the direction of gravity and respond by making the roots grow downward and the stem grow upward, has been widely studied in roots. The perception of gravity and the gravitational growth of roots, key steps in root growth and development, are regulated by auxins and other factors. Here, we review the latest progress in the regulation of root gravitropism by hormone signals and environmental factors from a molecular perspective, and look forward to the direction of future research on root gravitropism."
Authors: Alina Graf, Alkistis Eleftheria Lanassa Bassukas, Yao Xiao, Inês C. R. Barbosa, Julia Mergner, Peter Grill, Bernhard Michalke, Bernhard Kuster & Claus Schwechheimer
Editor's view: PIN-FORMED auxin transporters are activated by D6PK, the localization of which depends on cysteine S-acylation. Phosphorylation by PDKs regulates D6PK transport and residence time, and prevents lateral diffusion, revealing novel mechanisms for membrane interaction and polarity.
Authors: "D6 PROTEIN KINASE (D6PK) is a polarly localized plasma-membrane-associated kinase from Arabidopsis thaliana that activates polarly distributed PIN-FORMED auxin transporters. D6PK moves rapidly to and from the plasma membrane, independent of its PIN-FORMED targets. The middle D6PK domain, an insertion between kinase subdomains VII and VIII, is required and sufficient for association and polarity of the D6PK plasma membrane. How D6PK polarity is established and maintained remains to be shown. Here we show that cysteines from repeated middle domain CXX(X)P motifs are S-acylated and required for D6PK membrane association. While D6PK S-acylation is not detectably regulated during intracellular transport, phosphorylation of adjacent serine residues, in part in dependence on the upstream 3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE, promotes D6PK transport, controls D6PK residence time at the plasma membrane and prevents its lateral diffusion. We thus identify new mechanisms for the regulation of D6PK plasma membrane interaction and polarity."
Authors: Hui Wang, Huayang Wang, Houzhou Liu, Tao Wan, Yalin Li, Ketong Zhang, Sergey Shabala, Xuewen Li, Yinglong Chen and Min Yu.
Plant Physiology and Biochemistry (2024)
Highlights • Al stress changed RSA via increasing root GSA of pea. • Exogenous auxin negatively influences the gravitropism of lateral roots by reducing the starch granules in the root tip and changing auxin polar transport. • Al stress changed RSA through the auxin pathway, which is related to the root gravitropic response of plants.
Abstract: "Aluminium (Al) toxicity stands out as a primary cause of crop failure in acidic soils. The root gravity setpoint angle (GSA), one of the important traits of the root system architecture (RSA), plays a pivotal role in enabling plants to adapt to abiotic stress. This study explored the correlation between GSA and Al stress using hydroponic culture with pea (Pisum sativum) plants. The findings revealed that under Al stress, GSA increased in newly developed lateral roots. Notably, this response remained consistent regardless of the treatment duration, extending for at least 3 days during the experiment. Furthermore, exposure to Al led to a reduction in both the size and quantity of starch granules, pivotal components linked to gravity perception. The accumulation of auxin in root transition zone increased. This variation was mirrored in the expression of genes linked to granule formation and auxin efflux, particularly those in the PIN-formed family. This developmental framework suggested a unique role for the root gravitropic response that hinges on starch granules and auxin transport, acting as mediators in the modulation of GSA under Al stress. Exogenous application of indole-3-acetic acid (IAA) and the auxin efflux inhibitor N-1-naphthylphthalamic acid (NPA) had an impact on the root gravitropic response to Al stress. The outcomes indicate that Al stress inhibited polar auxin transport and starch granule formation, the two processes crucial for gravitropism. This impairment led to an elevation in GSA and a reconfiguration of RSA. This study introduces a novel perspective on how plant roots react to Al toxicity, culminating in RSA modification in the context of acidic soil with elevated Al concentrations."
Authors: Manvi Sharma and Petra Marhava.
Current Opinion in Plant Biology (2023)
Abstract: "Plants have evolved robust adaptive mechanisms to withstand the ever-changing environment. Tightly regulated distribution of the hormone auxin throughout the plant body controls an impressive variety of developmental processes that tailor plant growth and morphology to environmental conditions. The proper flow and directionality of auxin between cells is mainly governed by asymmetrically localized efflux carriers – PINs – ensuring proper coordination of developmental processes in plants. Discerning the molecular players and cellular dynamics involved in the establishment and maintenance of PINs in specific membrane domains, as well as their ability to readjust in response to abiotic stressors is essential for understanding how plants balance adaptability and stability. While much is known about how PINs get polarized, there is still limited knowledge about how abiotic stresses alter PIN polarity by acting on these systems. In this review, we focus on the current understanding of mechanisms involved in (re)establishing and maintaining PIN polarity under abiotic stresses."
Authors: Chong Yang, Huihui Wang, Qiqi Ouyang, Guo Chen, Xiaoyu Fu, Dianyun Hou and Huawei Xu.
Plants (2023)
Abstract: "Significant progress has been made in the functions of auxin efflux transporter PIN-FORMED (PIN) genes for the regulation of growth and development in rice. However, knowledge on the roles of OsPIN genes in abiotic stresses is limited. We previously reported that the mutation of OsPIN1b alters rice architecture and root gravitropism, while the role of OsPIN1b in the regulation of rice abiotic stress adaptations is still largely elusive. In the present study, two homozygous ospin1b mutants (C1b-1 and C1b-2) were employed to investigate the roles of OsPIN1b in regulating abiotic stress adaptations. Low temperature gradually suppressed OsPIN1b expression, while osmotic stress treatment firstly induced and then inhibited OsPIN1b expression. Most OsPIN genes and auxin biosynthesis key genes OsYUC were up-regulated in ospin1b leaves, implying that auxin homeostasis is probably disturbed in ospin1b mutants. The loss of function of OsPIN1b significantly decreased rice chilling tolerance, which was evidenced by decreased survival rate, increased death cells and ion leakage under chilling conditions. Compared with the wild-type (WT), ospin1b mutants accumulated more hydrogen peroxide (H2O2) and less superoxide anion radicals (O−2) after chilling treatment, indicating that reactive oxygen species (ROS) homeostasis is disrupted in ospin1b mutants. Consistently, C-repeat binding factor (CBF)/dehydration-responsive element binding factor (DREB) genes were downregulated in ospin1b mutants, implying that OsDREB genes are implicated in OsPIN1b-mediated chilling impairment. Additionally, the mutation of OsPIN1b led to decreased sensitivity to abscisic acid (ABA) treatment in seed germination, impaired drought tolerance in the seedlings and changed expression of ABA-associated genes in rice roots. Taken together, our investigations revealed that OsPIN1b is implicated in chilling and drought tolerance in rice and provide new insight for improving abiotic stress tolerance in rice."
Authors: Michael Mudgett, Zhouxin Shen, Xinhua Dai, Steven P. Briggs and Yunde Zhao.
PNAS (2023)
Significance: PIN auxin transporters and the PID (PINOID) kinase specify plant morphogenesis and organ formation by regulating dynamic gradients of the hormone auxin. Single pin1 (PIN-FORMED 1) or pid mutants produce pin-like inflorescences without functional flowers while double mutants often lack cotyledons and do not grow past the seedling stage. Surprisingly, we found that pid mutants produced fertile flowers when a single copy of PIN1 was mutated, suggesting that PID activity is obviated by reduced PIN1 gene dosage. The finding of PIN1 haplocomplementation of pid indicates that a multi-subunit complex which is sensitive to PIN1 levels is essential for flower initiation. Further study into this complex using the genetic materials presented here will uncover the exact mechanisms by which auxin regulates floral organogenesis.
Abstract: "Disruption of either the auxin transporter PIN-FORMED 1 (PIN1) or the protein kinase PINOID (PID) leads to the development of pin-like inflorescences. Previous studies have shown that phosphoregulation of PIN1 by AGC kinases including PID directs auxin flux to drive organ initiation. Here, we report unexpected findings on the genetic interactions between these two genes. We deleted the first 2/3 of the PIN1 coding sequence using CRISPR/Cas9, and the resulting pin1 mutant (pin1-27) was a strong allele. Surprisingly, heterozygous pin1-27 suppressed two independent pid null mutants, whereas homozygous pin1-27 enhanced the phenotypes of the pid mutants during embryogenesis. Furthermore, we show that deletion of either the hydrophilic loop or the second half of PIN1 also abolished PIN1 function, yet those heterozygous pin1 mutants were also capable of rescuing pid nulls. Moreover, we inserted green fluorescent protein (GFP) into the hydrophilic loop of PIN1 through CRISPR-mediated homology-directed repair (HDR). The GFP signal and pattern in the PIN1-GFPHDR line are similar to those in the previously reported PIN1-GFP transgenic lines. Interestingly, the PIN1-GFPHDR line also rescued various pid null mutant alleles in a semidominant fashion. We conclude that decreasing the number of functional PIN1 copies is sufficient to suppress the pid mutant phenotype, suggesting that PIN1 is likely part of a larger protein complex required for organogenesis."
Authors: Kwang-Ho Maeng, Hyodong Lee and Hyung-Taeg Cho.
PNAS (2023)
Significance: Phosphatidylinositol kinases are instrumental in endomembrane cargo trafficking by altering local membrane-lipid properties, and PIN-FORMED (PIN) auxin efflux transporters exhibit dynamic intracellular trafficking patterns modulated by the phosphorylation of their hydrophilic loop (HL) domain. Yet, the mechanisms by which phosphatidylinositol kinase establishes the trafficking pathway and selectivity of cargo and how PIN-HL phosphorylation influences PIN trafficking remained enigmatic. This study unveils that FAB1C, a phosphatidylinositol-3-phosphate 5-kinase in Arabidopsis, interfaces directly with PIN-HL, orchestrating PIN's vacuolar trafficking in a PIN-HL phosphorylation-dependent manner. These findings offer a leap forward in deciphering the interplay between membrane-lipid modifiers and cargo selection for endomembrane trafficking and the role of PIN phosphorylation in trafficking, enhancing our understanding of complex eukaryotic cellular processes.
Abstract: "PIN-FORMEDs (PINs) are auxin efflux carriers that asymmetrically target the plasma membrane (PM) and are critical for forming local auxin gradients and auxin responses. While the cytoplasmic hydrophilic loop domain of PIN (PIN-HL) is known to include some molecular cues (e.g., phosphorylation) for the modulation of PIN’s intracellular trafficking and activity, the complexity of auxin responses suggests that additional regulatory modules may operate in the PIN-HL domain. Here, we have identified and characterized a PIN-HL-interacting protein (PIP) called FORMATION OF APLOID AND BINUCLEATE CELL 1C (FAB1C), a phosphatidylinositol-3-phosphate 5-kinase, which modulates PIN's lytic trafficking. FAB1C directly interacts with PIN-HL and is required for the polarity establishment and vacuolar trafficking of PINs. Unphosphorylated forms of PIN2 interact more readily with FAB1C and are more susceptible to vacuolar lytic trafficking compared to phosphorylated forms. FAB1C also affected lateral root formation by modulating the abundance of periclinally localized PIN1 and auxin maximum in the growing lateral root primordium. These findings suggest that a membrane-lipid modifier can target the cargo-including vesicle by directly interacting with the cargo and modulate its trafficking depending on the cargo’s phosphorylation status."
Authors: Monika Dalal, Mansi and Karthikeyan Mayandi.
Planta (2023)
Main conclusion: The review describes tissue-specific and non-cell autonomous molecular responses regulating the root system architecture and function in plants.
Abstract: "Phenotypic plasticity of roots relies on specific molecular and tissue specific responses towards local and microscale heterogeneity in edaphic factors. Unlike gravitropism, hydrotropism in Arabidopsis is regulated by MIZU KUSSIE1 (MIZ1)-dependent asymmetric distribution of cytokinin and activation of Arabidopsis response regulators, ARR16 and ARR17 on the lower water potential side of the root leading to higher cell division and root bending. The cortex specific role of Abscisic acid (ABA)-activated SNF1-related protein kinase 2.2 (SnRK2.2) and MIZ1 in elongation zone is emerging for hydrotropic curvature. Halotropism involves clathrin-mediated internalization of PIN FORMED 2 (PIN2) proteins at the side facing higher salt concentration in the root tip, and ABA-activated SnRK2.6 mediated phosphorylation of cortical microtubule-associated protein Spiral2-like (SP2L) in the root transition zone, which results in anisotropic cell expansion and root bending away from higher salt. In hydropatterning, Indole-3-acetic acid 3 (IAA3) interacts with SUMOylated-ARF7 (Auxin response factor 7) and prevents expression of Lateral organ boundaries-domain 16 (LBD16) in air-side of the root, while on wet side of the root, IAA3 cannot repress the non-SUMOylated-ARF7 thereby leading to LBD16 expression and lateral root development. In root vasculature, ABA induces expression of microRNA165/microRNA166 in endodermis, which moves into the stele to target class III Homeodomain leucine zipper protein (HD-ZIP III) mRNA in non-cell autonomous manner. The bidirectional gradient of microRNA165/6 and HD-ZIP III mRNA regulates xylem patterning under stress. Understanding the tissue specific molecular mechanisms regulating the root responses under heterogeneous and stress environments will help in designing climate-resilient crops."
Authors: Robert D. Hill, Abir U. Igamberdiev and Claudio Stasolla.
Planta (2023)
Main conclusion: The preservation of quiescent center stem cell integrity in hypoxic roots by phytoglobins is exercised through their ability to scavenge nitric oxide and attenuate its effects on auxin transport and cell degradation. Under low oxygen stress, the retention or induction of phytoglobin expression maintains cell viability while loss or lack of induction of phytoglobin leads to cell degradation.
Abstract: "Plants have evolved unique attributes to ensure survival in the environment in which they must exist. Common among the attributes is the ability to maintain stem cells in a quiescent (or low proliferation) state in unfriendly environments. From the seed embryo to meristematic regions of the plant, quiescent stem cells exist to regenerate the organism when environmental conditions are suitable to allow plant survival. Frequently, plants dispose of mature cells or organs in the process of acclimating to the stresses to ensure survival of meristems, the stem cells of which are capable of regenerating cells and organs that have been sacrificed, a feature not generally available to mammals. Most of the research on plant stress responses has dealt with how mature cells respond because of the difficulty of specifically examining plant meristem responses to stress. This raises the question as to whether quiescent stem cells behave in a similar fashion to mature cells in their response to stress and what factors within these critical cells determine whether they survive or degrade when exposed to environmental stress. This review attempts to examine this question with respect to the quiescent center (QC) stem cells of the root apical meristem. Emphasis is put on how varying levels of nitric oxide, influenced by the expression of phytoglobins, affect QC response to hypoxic stress."
Authors: Rameshwar Sharma and Yellamaraju Sreelakshmi.
Journal of Experimental Botany (2023)
Abstract: "Axillary buds (ABs) are dormant buds located in the leaf axils of plants, which have the potential to develop into branches or flowers under appropriate conditions. At the molecular-genetic level, the miR156/SPL/SPB module regulates the development of ABs in plants, thus influencing plant architecture. Auxins are plant hormones that regulate various aspects of plant growth and development, including AB activity. Barrera-Rojas et al. (2023) show that suppressing AB outgrowth elevates auxin levels and lowers GOBLET expression, probably by suppressing its transcription by SBP15. Their findings provide insights into the regulation of AB outgrowth and tomato shoot architecture."
Authors: Zhongtao Jia, Ricardo F.H. Giehl, Anja Hartmann, Jose M. Estevez, Malcolm J. Bennett and Nicolaus von Wirén.
Current Biology (2023)
Editor's view: Jia et al. provide a mechanistic framework for hormone-regulated nutrient sensing in plants. They show that nitrogen deficiency activates a spatially defined auxin signaling cascade to promote the elongation of root hairs. This so-called foraging response allows better growth on nitrogen-poor substrates.
Highlights: • Plants elongate root hairs to ensure better growth in nitrogen-poor soil • Low N triggers expression of TAA1 and YUC8 to increase auxin levels in root tips • AUX1- and PIN2-mediated auxin transport activates ARF6/8 in the root hair zone • The regulatory module RHD6-LRL3 is required to elongate root hairs under low N
Abstract: "As a major determinant of the nutrient-acquiring root surface, root hairs (RHs) provide a low-input strategy to enhance nutrient uptake. Although primary and lateral roots exhibit elongation responses under mild nitrogen (N) deficiency, the foraging response of RHs and underlying regulatory mechanisms remain elusive. Employing transcriptomics and functional studies revealed a framework of molecular components composing a cascade of auxin synthesis, transport, and signaling that triggers RH elongation for N acquisition. Through upregulation of Tryptophan Aminotransferase of Arabidopsis 1 (TAA1) and YUCCA8, low N increases auxin accumulation in the root apex. Auxin is then directed to the RH differentiation zone via the auxin transport machinery, AUXIN TRANSPORTER PROTEIN 1 (AUX1) and PIN-FORMED 2 (PIN2). Upon arrival to the RH zone, auxin activates the transcription factors AUXIN RESPONSE FACTOR 6 and 8 (ARF6/8) to promote the epidermal and auxin-inducible transcriptional module ROOT HAIR DEFECTIVE 6 (RHD6)-LOTUS JAPONICA ROOT HAIRLESS-LIKE 3 (LRL3) to steer RH elongation in response to low N. Our study uncovers a spatially defined regulatory signaling cascade for N foraging by RHs, expanding the mechanistic framework of hormone-regulated nutrient sensing in plant roots."
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