25 Years of thermomorphogenesis research: milestones and perspectives.

In 1998, Bill Gray and colleagues showed that warm temperatures trigger arabidopsis hypocotyl elongation in an auxin-dependent manner. This laid the foundation for a vibrant research discipline. With several active members of the 'thermomorphogenesis' community, we here reflect on 25 years of elevated ambient temperature research and look to the future.

Deep inside the epigenetic memories of stressed plants.

Recent evidence sheds light on the peculiar type of plant intelligence. Plants have developed complex molecular networks that allow them to remember, choose, and make decisions depending on the stress stimulus, although they lack a nervous system. Being sessile, plants can exploit these networks to optimize their resources cost-effectively and maximize their fitness in response to multiple environmental stresses. Even more interesting is the capability to transmit this experience to the next generation(s) through epigenetic modifications that add to the classical genetic inheritance. In this opinion article, we present concepts and perspectives regarding the capabilities of plants to sense, perceive, remember, re-elaborate, respond, and to some extent transmit to their progeny information to adapt more efficiently to climate change.

Natural and induced epigenetic variation for crop improvement.

Maintaining global food security is a major challenge that requires novel strategies for crop improvement. Epigenetic regulation of plant responses to adverse environmental conditions provides a tunable mechanism to optimize plant growth, adaptation and ultimately yield. Epibreeding employs agricultural practices that rely on key epigenetic features as a means of engineering favorable phenotypic traits in target crops. This review summarizes recent findings on the role of epigenetic marks such as DNA methylation and histone modifications, in controlling phenotypic variation in crop species in response to environmental factors. The potential use of natural and induced epigenetic features as platforms for crop improvement via epibreeding, is discussed.

Light, chromatin, action: nuclear events regulating light signaling in Arabidopsis.

The plant nucleus provides a major hub for environmental signal integration at the chromatin level. Multiple light signaling pathways operate and exchange information by regulating a large repertoire of gene targets that shape plant responses to a changing environment. In addition to the established role of transcription factors in triggering photoregulated changes in gene expression, there are eminent reports on the significance of chromatin regulators and nuclear scaffold dynamics in promoting light-induced plant responses. Here, we report and discuss recent advances in chromatin-regulatory mechanisms modulating plant architecture and development in response to light, including the molecular and physiological roles of key modifications such as DNA, RNA and histone methylation, and/or acetylation. The significance of the formation of biomolecular condensates of key light signaling components is discussed and potential applications to agricultural practices overviewed.

TANDEM ZINC-FINGER/PLUS3 regulates phytochrome B abundance and signaling to fine-tune hypocotyl growth.

TANDEM ZINC-FINGER/PLUS3 (TZP) is a transcriptional regulator that acts at the crossroads of light and photoperiodic signaling. Here, we unveil a role for TZP in fine-tuning hypocotyl elongation under red light and long-day conditions. We provide genetic evidence for a synergistic action between TZP and PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1) in regulating the protein abundance of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and downstream gene expression in response to red light and long days (LDs). Furthermore, we show that TZP is a positive regulator of the red/far-red light receptor and thermosensor phytochrome B (phyB) by promoting phyB protein abundance, nuclear body formation, and signaling. Our data therefore assign a function to TZP in regulating two key red light signaling components, phyB and PIF4, but also uncover a new role for PCH1 in regulating hypocotyl elongation in LDs. Our findings provide a framework for the understanding of the mechanisms associated with the TZP signal integration network and their importance for optimizing plant growth and adaptation to a changing environment.

Low Fluence Ultraviolet-B Promotes Ultraviolet Resistance 8-Modulated Flowering in Arabidopsis.

Ultraviolet-B (UV-B) irradiation (280-320 nm) is an integral part of sunlight and a pivotal environmental cue that triggers various plant responses, from photoprotection to photomorphogenesis and metabolic processes. UV-B is perceived by ULTRAVIOLET RESISTANCE 8 (UVR8), which orchestrates UV-B signal transduction and transcriptional control of UV-B-responsive genes. However, there is limited information on the molecular mechanism underlying the UV-B- and UVR8-dependent regulation of flowering time in plants. Here, we investigate the role of UV-B and UVR8 in photoperiodic flowering in Arabidopsis thaliana. Our findings suggest that UV-B controls photoperiodic flowering in an ecotype-specific manner and that UVR8 acts as a negative regulator of UV-B-induced flowering. Overall, our research shows that UV-B modulates flowering initiation through the action of UVR8 at the transcriptional level.

An Epigenetic Alphabet of Crop Adaptation to Climate Change.

Crop adaptation to climate change is in a part attributed to epigenetic mechanisms which are related to response to abiotic and biotic stresses. Although recent studies increased our knowledge on the nature of these mechanisms, epigenetics remains under-investigated and still poorly understood in many, especially non-model, plants, Epigenetic modifications are traditionally divided into two main groups, DNA methylation and histone modifications that lead to chromatin remodeling and the regulation of genome functioning. In this review, we outline the most recent and interesting findings on crop epigenetic responses to the environmental cues that are most relevant to climate change. In addition, we discuss a speculative point of view, in which we try to decipher the "epigenetic alphabet" that underlies crop adaptation mechanisms to climate change. The understanding of these mechanisms will pave the way to new strategies to design and implement the next generation of cultivars with a broad range of tolerance/resistance to stresses as well as balanced agronomic traits, with a limited loss of (epi)genetic variability.

The Epigenetic Mechanisms Underlying Thermomorphogenesis and Heat Stress Responses in Arabidopsis.

Integration of temperature cues is crucial for plant survival and adaptation. Global warming is a prevalent issue, especially in modern agriculture, since the global rise in average temperature is expected to impact crop productivity worldwide. Hence, better understanding of the mechanisms by which plants respond to warmer temperatures is very important. This review focuses on the epigenetic mechanisms implicated in plant responses to high temperature and distinguishes the different epigenetic events that occur at warmer average temperatures, leading to thermomorphogenic responses, or subjected to extreme warm temperatures, leading to heat stress.

Epigenetics for Crop Improvement in Times of Global Change.

Epigenetics has emerged as an important research field for crop improvement under the on-going climatic changes. Heritable epigenetic changes can arise independently of DNA sequence alterations and have been associated with altered gene expression and transmitted phenotypic variation. By modulating plant development and physiological responses to environmental conditions, epigenetic diversity-naturally, genetically, chemically, or environmentally induced-can help optimise crop traits in an era challenged by global climate change. Beyond DNA sequence variation, the epigenetic modifications may contribute to breeding by providing useful markers and allowing the use of epigenome diversity to predict plant performance and increase final crop production. Given the difficulties in transferring the knowledge of the epigenetic mechanisms from model plants to crops, various strategies have emerged. Among those strategies are modelling frameworks dedicated to predicting epigenetically controlled-adaptive traits, the use of epigenetics for in vitro regeneration to accelerate crop breeding, and changes of specific epigenetic marks that modulate gene expression of traits of interest. The key challenge that agriculture faces in the 21st century is to increase crop production by speeding up the breeding of resilient crop species. Therefore, epigenetics provides fundamental molecular information with potential direct applications in crop enhancement, tolerance, and adaptation within the context of climate change.

Deciphering the Epigenetic Alphabet Involved in Transgenerational Stress Memory in Crops.

Although epigenetic modifications have been intensely investigated over the last decade due to their role in crop adaptation to rapid climate change, it is unclear which epigenetic changes are heritable and therefore transmitted to their progeny. The identification of epigenetic marks that are transmitted to the next generations is of primary importance for their use in breeding and for the development of new cultivars with a broad-spectrum of tolerance/resistance to abiotic and biotic stresses. In this review, we discuss general aspects of plant responses to environmental stresses and provide an overview of recent findings on the role of transgenerational epigenetic modifications in crops. In addition, we take the opportunity to describe the aims of EPI-CATCH, an international COST action consortium composed by researchers from 28 countries. The aim of this COST action launched in 2020 is: (1) to define standardized pipelines and methods used in the study of epigenetic mechanisms in plants, (2) update, share, and exchange findings in epigenetic responses to environmental stresses in plants, (3) develop new concepts and frontiers in plant epigenetics and epigenomics, (4) enhance dissemination, communication, and transfer of knowledge in plant epigenetics and epigenomics.

Wavelength-dependent effects of artificial light at night on phytoplankton growth and community structure.

Artificial light at night (ALAN) is a disruptive form of pollution, impacting physiological and behavioural processes that may scale up to population and community levels. Evidence from terrestrial habitats show that the severity and type of impact depend on the wavelength and intensity of ALAN; however, research on marine organisms is still limited. Here, we experimentally investigated the effect of different ALAN colours on marine primary producers. We tested the effect of green (525 nm), red (624 nm) and broad-spectrum white LED ALAN, compared to a dark control, on the green microalgae Tetraselmis suesica and a diatom assemblage. We show that green ALAN boosted chlorophyll production and abundance in T. suesica. All ALAN wavelengths affected assemblage biomass and diversity, with red and green ALAN having the strongest effects, leading to higher overall abundance and selective dominance of specific diatom species, some known to cause harmful algal blooms. Our findings show that green and red ALAN should be used with caution as alternative LED colours in coastal areas, where there might be a need to strike a balance between the effects of green and red light on marine primary producers with the benefit they appear to bring to other organisms.

Photobody Detection Using Immunofluorescence and Super-Resolution Imaging in Arabidopsis.

Light triggers changes in plant nuclear architecture to control differentiation, adaptation, and growth. A series of genetic, molecular, and imaging approaches have revealed that the nucleus forms a hub for photo-induced protein interactions and gene regulatory events. However, the mechanism and function of light-induced nuclear compartmentalization is still unclear. This chapter provides detailed experimental protocols for examining the morphology and potential functional significance of light signaling components that localize in light-induced subnuclear domains, also known as photobodies. We describe how immunolabeling of endogenous proteins and fluorescent in situ hybridization (FISH) could be combined with confocal imaging of fluorescently tagged proteins to assess co-localization in Arabidopsis nuclei. Furthermore, we employ a super-resolution imaging approach to study the morphology of photobodies at unprecedented detail.

How to build an effective research network: lessons from two decades of the GARNet plant science community.

Successful collaborative research is dependent on excellent ideas and innovative experimental approaches, as well as the provision of appropriate support networks. Collaboration requires venues, infrastructures, training facilities, and, perhaps most importantly, a sustained commitment to work together as a community. These activities do not occur without significant effort, yet can be facilitated and overseen by the leadership of a research network that has a clearly defined role to help build resources for their community. Over the past 20 years, this is a role that the UKRI-BBSRC-funded GARNet network has played in the support of the UK curiosity-driven, discovery-led plant science research community. This article reviews the lessons learnt by GARNet in the hope that they can inform the practical implementation of current and future research networks.

CIPK23 regulates blue light-dependent stomatal opening in Arabidopsis thaliana.

Phototropins (phot1 and phot2) are plant blue light receptor kinases that function to mediate phototropism, chloroplast movement, leaf flattening, and stomatal opening in Arabidopsis. Considerable progress has been made in understanding the mechanisms associated with phototropin receptor activation by light. However, the identities of phototropin signaling components are less well understood by comparison. In this study, we specifically searched for protein kinases that interact with phototropins by using an in vitro screening method (AlphaScreen) to profile interactions against an Arabidopsis protein kinase library. We found that CBL-interacting protein kinase 23 (CIPK23) interacts with both phot1 and phot2. Although these interactions were verified by in vitro pull-down and in vivo bimolecular fluorescence complementation assays, CIPK23 was not phosphorylated by phot1, as least in vitro. Mutants lacking CIPK23 were found to exhibit impaired stomatal opening in response to blue light but no deficits in other phototropin-mediated responses. We further found that blue light activation of inward-rectifying K+ (K+ in ) channels was impaired in the guard cells of cipk23 mutants, whereas activation of the plasma membrane H+ -ATPase was not. The blue light activation of K+ in channels was also impaired in the mutant of BLUS1, which is one of the phototropin substrates in guard cells. We therefore conclude that CIPK23 promotes stomatal opening through activation of K+ in channels most likely in concert with BLUS1, but through a mechanism other than activation of the H+ -ATPase. The role of CIPK23 as a newly identified component of phototropin signaling in stomatal guard cells is discussed.

The diverse and unanticipated roles of histone deacetylase 9 in coordinating plant development and environmental acclimation.

Plants tightly control gene transcription to adapt to environmental conditions and steer growth and development. Different types of epigenetic modifications are instrumental in these processes. In recent years, an important role for the chromatin-modifying RPD3/HDA1 class I HDAC HISTONE DEACETYLASE 9 (HDA9) emerged in the regulation of a multitude of plant traits and responses. HDACs are widely considered transcriptional repressors and are typically part of multiprotein complexes containing co-repressors, DNA, and histone-binding proteins. By catalyzing the removal of acetyl groups from lysine residues of histone protein tails, HDA9 negatively controls gene expression in many cases, in concert with interacting proteins such as POWERDRESS (PWR), HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 15 (HOS15), WRKY53, ELONGATED HYPOCOTYL 5 (HY5), ABA INSENSITIVE 4 (ABI4), and EARLY FLOWERING 3 (ELF3). However, HDA9 activity has also been directly linked to transcriptional activation. In addition, following the recent breakthrough discovery of mutual negative feedback regulation between HDA9 and its interacting WRKY-domain transcription factor WRKY53, swift progress in gaining understanding of the biology of HDA9 is expected. In this review, we summarize knowledge on this intriguing versatile-and long under-rated-protein and propose novel leads to further unravel HDA9-governed molecular networks underlying plant development and environmental biology.

The impact of light and temperature on chromatin organization and plant adaptation.

Light and temperature shape the developmental trajectory and morphology of plants. Changes in chromatin organization and nuclear architecture can modulate gene expression and lead to short- and long-term plant adaptation to the environment. Here, we review recent reports investigating how changes in chromatin composition, structure, and topology modulate gene expression in response to fluctuating light and temperature conditions resulting in developmental and physiological responses. Furthermore, the potential application of novel revolutionary techniques, such Hi-C, RNA fluorescence in situ hybridization (FISH) and padlock-FISH, to study the impact of environmental stimuli such as light and temperature on nuclear compartmentalization in plants is discussed.

Let it bloom: cross-talk between light and flowering signaling in Arabidopsis.

The terrestrial environment is complex, with many parameters fluctuating on daily and seasonal basis. Plants, in particular, have developed complex sensory and signaling networks to extract and integrate information about their surroundings in order to maximize their fitness and mitigate some of the detrimental effects of their sessile lifestyles. Light and temperature each provide crucial insights on the surrounding environment and, in combination, allow plants to appropriately develop, grow and adapt. Cross-talk between light and temperature signaling cascades allows plants to time key developmental decisions to ensure they are 'in sync' with their environment. In this review, we discuss the major players that regulate light and temperature signaling, and the cross-talk between them, in reference to a crucial developmental decision faced by plants: to bloom or not to bloom?

HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion.

Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatin-modifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.

Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake.

Phytoplankton face environmental nutrient variations that occur in the dynamic upper layers of the ocean. Phytoplankton cells are able to rapidly acclimate to nutrient fluctuations by adjusting their nutrient-uptake system and metabolism. Disentangling these acclimation responses is a critical step in bridging the gap between phytoplankton cellular physiology and community ecology. Here, we analyzed the dynamics of phosphate (P) uptake acclimation responses along different P temporal gradients by using batch cultures of the diatom Phaeodactylum tricornutum. We employed a multidisciplinary approach that combined nutrient-uptake bioassays, transcriptomic analysis, and mathematical models. Our results indicated that cells increase their maximum nutrient-uptake rate (Vmax) both in response to P pulses and strong phosphorus limitation. The upregulation of three genes coding for different P transporters in cells experiencing low intracellular phosphorus levels supported some of the observed Vmax variations. In addition, our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at medium-high environmental and low intracellular phosphorus levels, respectively. Our results highlight the existence of a sequence of acclimation stages along the phosphate continuum that can be understood as a succession of acclimation responses. We provide a novel conceptual framework that can contribute to integrating and understanding the dynamics and wide diversity of acclimation responses developed by phytoplankton.