Search bioRxiv⌕ Search

Biology subjects

van Veen, H.

Publications and source records attributed to van Veen, H..

11 recordsLinked to original sources

Leaf-age specific flood resilience in Arabidopsis thaliana is determined by distinct processes contributing to post-submergence recovery

While the molecular mechanisms mediating submergence tolerance have been extensively studied, those underpinning age-dependent resilience remain poorly characterized. In Arabidopsis thaliana, submergence elicits a leaf-age dependent phenotype in which senescence and death progress across an age gradient starting with older leaves. Here we sought to investigate the mechanisms mediating this observed differential flood resilience by interrogating leaf age-specific transcriptome and proteome changes during submergence and recovery. Following submergence, most age-dependent differences were in the magnitude or speed of transcript abundance changes, whereas qualitative leaf-age dependent responses were most apparent during recovery. This included a strong desiccation response in old leaves despite a stronger ABA-signaling response. Physiological measurements suggested that faster dehydration was facilitated by a combination of submergence-mediated reduction of ABA sensitivity and higher conductance in old leaves. We also observed a stronger induction in young shoot tissue of genes associated with endoplasmic reticulum (ER) stress and the unfolded protein response (UPR). Mutants disabled in the two UPR signaling branches were affected in new leaf formation and the ability to restore the proteome, but not in senescence, suggesting that young tissues activate ER stress recovery to permit continuation of growth. Of the mitochondrial membrane proteins differentially regulated in young leaves, loss of mitochondrial voltage-dependent anion channel function impacted submergence-recovery tolerance. Our data reveal multiple mechanisms underlying leaf age-dependent differential submergence recovery and demonstrate how tolerance is determined by an interplay between age related developmental traits and stress signaling pathways.

plant biology↗

The role of ERFVIIs as oxygen-sensing transducers in the evolution of land plant response to hypoxia

The transcriptional response to low oxygen (hypoxia) in the flowering plant Arabidopsis thaliana is transduced through group VII Ethylene Response Factor (ERFVII) transcription factors, whose proteolysis is oxygen-dependent via the PLANT CYSTEINE OXIDASE (PCO) N-degron pathway. When and how this response to hypoxia evolved in land plants remains unknown. Here we investigated the conservation and divergence of transcriptional responses to hypoxia in major land plant clades. We identified induction of gene functions associated with glycolysis and fermentation as part of a conserved response across all land plant divisions. Our results indicate that ERFVIIs appeared in the last common ancestor of vascular plants with true roots, concurrently with oxygen-dependent destabilisation, to regulate hypoxia-adaptive genes. Proteins from other ERF groups have been recruited multiple times in different clades as substrates of the PCO N-degron pathway. Our results demonstrate that the response of land plants to hypoxia has been refined in derived clades through the evolution of ERFVIIs as transcriptional transducers, that occurred concomitantly with the appearance of vascular systems and roots as foraging systems through hypoxic soil.

plant biology↗

Phylotranscriptomics provides a treasure trove of flood tolerance mechanisms in the Cardamineae tribe

Flooding events are highly detrimental to most terrestrial plant species. However, there is an impressive diversity of plant species that thrive in flood-prone regions and represent a treasure trove of unexplored flood-resilience mechanisms. Here we surveyed a panel of four species from the Cardamineae tribe representing a broad tolerance range. This included the flood-tolerant Cardamine pratensis, Rorippa sylvestris and Rorippa palustris and the flood-sensitive species Cardamine hirsuta. All four species displayed a quiescent strategy, evidenced by the repression of shoot growth underwater. Comparative transcriptomics analyses between the four species and the sensitive model species Arabidopsis thaliana were facilitated via de-novo transcriptome assembly and identification of 16,902 universal orthogroups at a high resolution. Our results suggest that tolerance likely evolved separately in the Cardamine and Rorippa species. While the Rorippa response was marked by a strong downregulation of cell-cycle genes, Cardamine minimized overall transcriptional regulation. However, a weak starvation signature was a universal trait of tolerant species, potentially achieved in multiple ways. It could result from a strong decline in cell-cycle activity, but is also intertwined with autophagy, senescence, day-time photosynthesis and night-time fermentation capacity. Our dataset provides a rich source to study adaptational mechanisms of flooding tolerance.

plant biology↗

A low-cost and open-source imaging platform reveals spatiotemporal insight into Arabidopsis leaf elongation and movement

Plant organs move throughout the diurnal cycle, changing leaf and petiole positions to balance light capture, leaf temperature and water loss under dynamic environmental conditions. Upward movement of the petiole, called hyponasty, is one of several traits of the shade avoidance syndrome (SAS). SAS traits are elicited upon perception of vegetation shade signals such as far-red light (FR) and improve light capture in dense vegetation. Monitoring plant movement at a high temporal resolution allows studying functionality, as well as molecular regulation of hyponasty. However, high temporal resolution imaging solutions are often very expensive, making this unavailable to many researchers. Here, we present a modular and low-cost imaging set-up, based on small Raspberry Pi computers, that can track leaf movements and elongation growth with high temporal resolution. We also developed an open-source, semi-automated image analysis pipeline. Using this setup we followed responses to FR enrichment, light intensity and their interactions. Tracking both elongation and angle of petiole, lamina and entire leaf revealed insight into R:FR sensitivities of leaf growth and movement dynamics, and its interactions with background light intensity. We also identified spatial separation in hyponastic response regulation for the petiole and the lamina of the leaf, depending on the light conditions.

plant biology↗

Ethylene-mediated phosphorylation of ORESARA1 induces sequential leaf death during flooding in Arabidopsis

The volatile phytohormone ethylene is a major regulator of plant adaptive responses to flooding. In flooded plant tissues, it quickly increases to high concentrations due to its low solubility and diffusion rates in water. The passive, quick and consistent accumulation of ethylene in submerged plant tissues makes it a reliable cue to trigger flood-acclimative responses, including metabolic adjustments to cope with flood-induced hypoxia. However, persistent ethylene accumulation also accelerates leaf senescence. Stress-induced senescence hampers the photosynthetic capacity and stress recovery. In submerged Arabidopsis shoots, senescence follows a strict age-dependent pattern starting with the older leaves. Although mechanisms underlying ethylene-mediated senescence have been uncovered, it is unclear how submerged plants avoid an indiscriminate breakdown of leaves despite high systemic ethylene accumulation. Here we demonstrate in Arabidopsis plants that even though submergence triggers a leaf-age independent activation of ethylene signaling via EIN3, senescence was initiated only in the old leaves, and independent of the N-degron pathway of oxygen sensing. This EIN3 stabilization also led to the overall transcript and protein accumulation of the senescence-promoting transcription factor ORESARA1 (ORE1). ORE1 protein accumulated in both old and young leaves during submergence. However, leaf age-dependent senescence could be explained by ORE1 protein activation specifically in old leaves, independent of the previously identified age-dependent control of ORE1 via miR164. Our results unravel a mechanism by which plants regulate the speed and pattern of senescence during environmental stresses like flooding. The age-dependent activity of ORE1 ensures that older expendable leaves are dismantled first, thus prolonging the life of younger leaves and meristematic tissues vital to whole plant survival. Significance statementFlooded plants systemically accumulate saturating concentrations of the senescence promoting volatile hormone ethylene. Yet, leaf senescence follows a strict age-dependent gradient, thus prolonging the survival of young leaves and meristematic tissue. Here we show that in flooded plants, age-independent activation of ethylene signaling via EIN3, induces the systemic accumulation of the senescence-inducing transcription factor ORE1. Premature senescence of younger tissues is prevented by the posttranslational activation of ORE1 specifically in old leaves, where it induces the transcription of senescence-associated genes. Our results highlight how a systemic stress signal (ethylene accumulation upon flooding) induces a signaling cascade that diverges in an age-dependent manner, and eventually leads to an age-dependent physiological output (leaf senescence).

plant biology↗

Ethylene augments root hypoxia tolerance through amelioration of reactive oxygen species and growth cessation

Flooded plants experience impaired gas diffusion underwater, leading to oxygen deprivation (hypoxia). The volatile plant hormone ethylene is rapidly trapped in submerged plant cells and is instrumental for enhanced hypoxia acclimation. However, the precise mechanisms underpinning ethylene-enhanced hypoxia survival remain unclear. We studied the effect of ethylene pre-treatment on hypoxia survival of primary Arabidopsis thaliana root tips. Both hypoxia itself and re-oxygenation following hypoxia are highly damaging to root tip cells and ethylene pre-treatments reduced this damage. Ethylene pre-treatment alone altered the abundance of transcripts and proteins involved in hypoxia responses, root growth, translation and reactive oxygen species (ROS) homeostasis. Through imaging and manipulating ROS abundance in planta, we demonstrate that ethylene limits excessive ROS formation during hypoxia and subsequent re-oxygenation and improves oxidative stress survival. In addition, we show that ethylene leads to rapid root growth cessation and this quiescence behaviour contributes to enhanced hypoxia tolerance. Collectively, our results show that the early flooding signal ethylene modulates a variety of processes that all contribute to hypoxia survival.

plant biology↗

Towards increased shading potential: a combined phenotypic and genetic analysis of rice shoot architecture

Rice feeds more than half of the worlds human population. In modern rice farming, a major constraint for productivity is weed proliferation and the ecological impact of herbicide application. Increased weed competitiveness of commercial rice varieties requires enhanced shade casting to limit growth of shade-sensitive weeds and the need for herbicide. We aimed to identify traits that enhance rice shading capacity based on the canopy architecture and the underlying genetic components. We performed a phenotypic screen of a rice diversity panel comprised of 344 varieties, examining 13 canopy architecture traits linked with shading capacity in 4-week-old plants. The analysis revealed a vast range of phenotypic variation across the diversity panel. We used trait correlation and clustering to identify core traits that define shading capacity to be shoot area, number of leaves, culm and solidity (the compactness of the shoot). To simplify the complex canopy architecture, these traits were combined into a Shading Rank metric that is indicative of a plants ability to cast shade. Genome wide association study (GWAS) revealed genetic loci underlying canopy architecture traits, out of which five loci were substantially contributing to shading potential. Subsequent haplotype analysis further explored allelic variation and identified seven haplotypes associated with increased shading. Identification of traits contributing to shading capacity and underlying allelic variation presented in this study will serve future genomic assisted breeding programmes. The investigated diversity panel, including widely grown varieties, shows that there is big potential and genetic resources for improvement of elite breeding lines. Implementing increased shading in rice breeding will make its farming less dependent on herbicides and contribute towards more environmentally sustainable agriculture. One sentence summaryThrough screening a rice diversity panel for variation in shoot architecture, we identified traits corresponding to plant shading potential and their genetic constituents.

plant biology↗

Nighttime gibberellin biosynthesis is influenced by fluctuating environmental conditions and contributes to growth adjustments of Arabidopsis leaves.

Optimal plant growth performance requires that the action of growth signals, such as gibberellins (GA), are coordinated with the availability of photo-assimilates. Here, we studied the links between gibberellin biosynthesis and carbon availability, and the subsequent effects on growth. The results presented here show that carbon availability, light and dark cues, and the clock ensure the timing and magnitude of gibberellin biosynthesis and that disruption of these mechanisms results in reduced gibberellin levels and expression of downstream genes. Carbon dependent nighttime induction of GIBBERELLIN 3-BETA-DIOXYGENASE 1 (GA3ox1) was severely hampered when preceded by a day of lowered light availability, leading specifically to reduced bioactive GA4 levels, and coinciding with a decline in leaf expansion rate during the night. We attribute this decline in leaf expansion mostly to reduced photo-assimilates. However, plants where gibberellin limitation was alleviated had significantly improved expansion demonstrating the relevance of gibberellins in growth control under varying carbon availability. Carbon dependent expression of upstream gibberellin biosynthesis genes (KAURENE SYNTHASE, KS and GIBBERELLIN 20 OXIDASE 1, GA20ox1) was not translated into metabolite changes within this short timeframe. We propose a model where the extent of nighttime biosynthesis of bioactive GA4 by GA3ox1 is determined by starch, as the nighttime carbon source, and so provides day-to-day adjustment of gibberellin responses.

plant biology↗

Mitochondrial translation and dynamics synergistically extend lifespan in C. elegans through HLH-30

Mitochondrial form and function, such as translation, are closely interlinked in homeostasis and aging. Inhibiting mitochondrial translation is known to increase lifespan in C. elegans, which is accompanied by a fragmented mitochondrial network. However, the causality between mitochondrial translation and morphology in longevity remains uncharacterized. Here, we show in C. elegans that disrupting mitochondrial network homeostasis by either blocking fission or fusion synergizes with the reduced mitochondrial translation to substantially prolong lifespan and stimulate stress response such as the mitochondrial unfolded protein response, UPRMT. Conversely, immobilizing the mitochondrial network through a simultaneous abrogation of fission and fusion reverses the lifespan increase induced by mitochondrial translation inhibition. Furthermore, we find that the synergistic effect of inhibiting both mitochondrial translation and dynamics on lifespan, despite stimulating UPRMT, does not require it. Instead, this lifespan-extending synergy is exclusively dependent on the lysosome biogenesis and autophagy transcription factor HLH-30/TFEB. Altogether, our study reveals the mechanistic connections between mitochondrial translation and dynamics in regulating longevity. SUMMARYMitochondrial form and function are intimately intertwined. Liu et al. find the synergistic effect of inhibiting both mitochondrial translation and dynamics on lifespan. This synergy is dependent on the induction of lysosome biogenesis through the nuclear localization of HLH-30.

cell biology↗

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

Timely perception of adverse environmental changes is critical for survival. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced hypoxia. However, how plants detect and transduce early submergence signals remains elusive. Here we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent hypoxia. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies novel regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.

plant biology↗

A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

Abiotic stresses in plants are often transient and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG (RBOHD), SENESCENCE-ASSOCIATED GENE113 (SAG113) and ORESARA1 (ORE1/NAC6) which function in a regulatory network involving a reactive oxygen species (ROS) burst upon de-submergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to pre-stress homeostasis.\n\nSignificance statementFlooding due to extreme weather events can be highly detrimental to plant development and yield. Speedy recovery following stress removal is an important determinant of tolerance, yet mechanisms regulating this remain largely uncharacterized. We identified a regulatory network in Arabidopsis thaliana that controls water loss and senescence to influence recovery from prolonged submergence. Targeted control of the molecular mechanisms facilitating stress recovery identified here can potentially improve performance of crops in flood-prone areas.

plant biology↗