ORCID Profile
0000-0003-3554-7228
Current Organisation
Australian National University
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Plant Cell and Molecular Biology | Plant Biology | Plant Physiology |
Publisher: Oxford University Press (OUP)
Date: 19-05-2021
DOI: 10.1093/JXB/ERAB218
Abstract: The evolution of photosynthesis and its associated metabolic pathways has been crucial to the successful establishment of plants, but has also challenged plant cells in the form of production of reactive oxygen species (ROS). Intriguingly, multiple forms of ROS are generated in virtually every plant cell compartment through erse pathways. As a result, a sophisticated network of ROS detoxification and signaling that is simultaneously tailored to in idual organelles and safeguards the entire cell is necessary. Here we take an organelle-centric view on the principal sources and sinks of ROS across the plant cell and provide insights into the ROS-induced organelle to nucleus retrograde signaling pathways needed for operational readjustments during environmental stresses.
Publisher: Oxford University Press (OUP)
Date: 06-02-2017
DOI: 10.1104/PP.16.01494
Publisher: Oxford University Press (OUP)
Date: 10-2019
DOI: 10.1105/TPC.19.00272
Publisher: Oxford University Press (OUP)
Date: 27-02-2018
DOI: 10.1104/PP.17.01611
Publisher: Proceedings of the National Academy of Sciences
Date: 18-07-2016
Abstract: Management of oxidative stress in plant chloroplasts involves signaling pathways to the nucleus that trigger stress response mechanisms. Yet, how oxidative stress is initially sensed in the chloroplast to activate accumulation of a stress signal remains enigmatic. We show that inactivation of a phosphatase, SAL1, by oxidative stress in chloroplasts controls accumulation of its substrate, as a plant stress signal. This regulatory mechanism is highly conserved across the plant kingdom and confers a second function to this metabolic enzyme as an oxidative stress sensor.
Publisher: Proceedings of the National Academy of Sciences
Date: 25-02-2019
Abstract: Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3′-phosphoadenosine-5′-phosphate (PAP) metabolism, evolved in streptophyte algae—the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii , and the moss Physcomitrella patens . Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these erse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.
Publisher: Informa UK Limited
Date: 12-2010
Publisher: eLife Sciences Publications, Ltd
Date: 21-03-2017
DOI: 10.7554/ELIFE.23361
Abstract: Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3′-phosphoadenosine 5′- phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1) priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost1-2. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca2+ up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to fine-tune physiological responses.
Publisher: Cold Spring Harbor Laboratory
Date: 03-08-2023
DOI: 10.1101/2023.08.02.551742
Abstract: Cellular responses to abiotic stress involve multiple secondary messengers including reactive oxygen species (ROS), Ca 2+ , phytohormones such as abscisic acid (ABA) and chloroplast-to-nucleus retrograde signals such as 3’-phosphoadenosine 5’-phosphate (PAP). Mechanism(s) by which these messengers, produced in different subcellular compartments, intersect for cell regulation remain enigmatic. Here we demonstrate a mechanistic link enabling ABA and the chloroplast retrograde signal PAP to coordinate both chloroplast and plasma membrane ROS production. In whole leaves, PAP alters various ROS-related processes including plasmodesmal permeability as well as responses to ozone and the bacterial elicitor flg22, but largely quenches ROS during oxidative stress. Conversely, in guard cells, both PAP and ABA induce a ROS burst in both chloroplasts via photosynthetic electron transport, and the apoplast via the RESPIRATORY BURST OXIDASE HOMOLOG (RBOH). Both subcellular ROS sources were necessary for ABA- and PAP-mediated stomatal closure. However, PAP signaling erges from ABA by activating RBOHD, instead of RBOHF, for apoplastic ROS production. We identify calcium-dependent protein kinases (CPKs) transcriptionally induced by PAP as the post-translational activators of RBOHD-mediated ROS production. CPK13, CPK32, and CPK34 concurrently activate RBOHD and the slow anion channel SLAC1 by phosphorylating two Serine (S) residues, including S120 which is also targeted by the core ABA signaling kinase OPEN STOMATA 1 (OST1). Consequently, overexpressing the PAP-induced CPKs rescues stomatal closure in ost1. Our data identify chloroplasts, as sources and mediators of ROS and retrograde signals such PAP, to be critical environmental sensors and focal node in the multifaceted cellular stress response network. The chloroplast is an important node to coordinate multiple plant signaling pathways in response to stresses such as drought. However, how does it function in specialized cells for which carbon fixation is secondary? Here we show that the chloroplast retrograde signal 3’-phosphoadenosine 5’-phosphate (PAP) plays multiple roles in reactive oxygen species (ROS) signaling and homeostasis. While PAP suppresses ROS in photosynthetic tissue, surprisingly PAP induces ROS in chloroplasts and extracellular space of guard cells to induce stomatal closure. We decipher how PAP-induced proteins activate both extracellular ROS production and anion channels for stomatal closure, thus providing a mechanism by which chloroplasts provide a strategic complement to canonical hormonal pathways in regulating plant physiological responses in specialized cells.
Publisher: Proceedings of the National Academy of Sciences
Date: 17-03-2014
Abstract: A fundamental question in developmental biology is how patterns are established in space and time. In plants, key differences in root system architecture are attributed to the spatial distribution pattern of lateral roots (LRs), yet how the pattern of LRs is established is only beginning to be understood. We demonstrate that the establishment of sites competent to form LRs roots requires carotenoid biosynthesis. Furthermore, our results implicate an uncharacterized carotenoid-derived molecule that functions non–cell-autonomously, specifically in LR formation. The results of this study reveal novel aspects of carotenoid biology and expand the roles of carotenoid-derived molecules into root developmental patterning.
Publisher: Oxford University Press (OUP)
Date: 14-03-2019
DOI: 10.1093/JXB/ERZ119
Abstract: Secondary sulfur metabolism produces several metabolites which regulate various aspects of cellular signalling and homeostasis in response to environmental perturbations.
Publisher: Wiley
Date: 2018
DOI: 10.1002/PLD3.31
Abstract: Homeostasis of metabolism and regulation of stress‐signaling pathways are important for plant growth. The metabolite 3′‐phosphoadenosine‐5′‐phosphate (PAP) plays dual roles as a chloroplast retrograde signal during drought and high light stress, as well as a toxic by‐product of secondary sulfur metabolism, and thus, its levels are regulated by the chloroplastic phosphatase, SAL1. Constitutive PAP accumulation in sal1 mutants improves drought tolerance but can impair growth and alter rosette morphology. Therefore, it is of interest to derive strategies to enable controlled and targeted PAP manipulation that could enhance drought tolerance while minimizing the negative effects on plant growth. We systematically tested the potential and efficiency of multiple established transgenic manipulation tools in altering PAP levels in Arabidopsis. Dexamethasone (dex)‐inducible silencing of SAL1 via hpRNAi [pOpOff: SAL1 hpRNAi] yielded reduction in SAL1 transcript and protein levels, yet failed to significantly induce PAP accumulation. Surprisingly, this was not due to insufficient silencing of the inducible system, as constitutive silencing using a strong promoter to drive hpRNAi and amiRNA targeting the SAL1 transcript also failed to increase PAP content or induce a sal1 ‐like plant morphology despite significantly reducing the SAL1 transcript levels. In contrast, using dex‐inducible expression of SAL1 cDNA to complement an Arabidopsis sal1 mutant successfully modulated PAP levels and restored rosette growth in a dosage‐dependent manner. Results from this inducible complementation system indicate that plants with intermediate PAP levels could have improved rosette growth without compromising its drought tolerance. Additionally, preliminary evidence suggests that SAL1 cDNA driven by promoters of genes expressed specifically during early developmental stages such as ABA‐Insensitive 3 ( ABI3 ) could be another potential strategy for studying and optimizing PAP levels and drought tolerance while alleviating the negative impact of PAP on plant growth in sal1 . Thus, we have identified ways that can allow future dissection into multiple aspects of stress and developmental regulation mediated by this chloroplast signal.
Publisher: Annual Reviews
Date: 29-04-2016
DOI: 10.1146/ANNUREV-ARPLANT-043015-111854
Abstract: The chloroplast can act as an environmental sensor, communicating with the cell during biogenesis and operation to change the expression of thousands of proteins. This process, termed retrograde signaling, regulates expression in response to developmental cues and stresses that affect photosynthesis and yield. Recent advances have identified many signals and pathways—including carotenoid derivatives, isoprenes, phosphoadenosines, tetrapyrroles, and heme, together with reactive oxygen species and proteins—that build a communication network to regulate gene expression, RNA turnover, and splicing. However, retrograde signaling pathways have been viewed largely as a means of bilateral communication between organelles and nuclei, ignoring their potential to interact with hormone signaling and the cell as a whole to regulate plant form and function. Here, we discuss new findings on the processes by which organelle communication is initiated, transmitted, and perceived, not only to regulate chloroplastic processes but also to intersect with cellular signaling and alter physiological responses.
Publisher: Frontiers Media SA
Date: 08-08-2018
Publisher: Elsevier BV
Date: 2013
DOI: 10.1016/J.TPLANTS.2012.07.005
Abstract: A key plant response to drought is the accumulation of specific sets of metabolites that act as osmoprotectants, osmolytes, antioxidants, and/or stress signals. An emerging question is: how do plants regulate metabolism to balance the 'competing interests' between metabolites during stress? Recent research connects primary sulfur metabolism (e.g., sulfate transport in the vasculature, its assimilation in leaves, and the recycling of sulfur-containing compounds) with the drought stress response. In this review, we highlight key steps in sulfur metabolism that play significant roles in drought stress signaling and responses. We propose that a complex balancing act is required to coordinate primary and secondary sulfur metabolism during the drought stress response in plants.
Publisher: Frontiers Media SA
Date: 2013
Publisher: eLife Sciences Publications, Ltd
Date: 11-03-2017
Location: Belgium
Start Date: 02-2022
End Date: 02-2025
Amount: $427,623.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2022
End Date: 2025
Funder: Australian Research Council
View Funded ActivityStart Date: 2017
End Date: 2021
Funder: Research Foundation - Flanders
View Funded Activity