Plants exhibit striking developmental plasticity, driven by stem cell populations within meristematic tissues such as the shoot apical meristem (SAM). While the genetic networks governing stem cell homeostasis are well-characterized, recent studies reveal that the SAM also functions as an active environmental sensor to modulate growth plasticity. This Tansley review synthesizes advances in how the SAM perceives and integrates key environmental signals - including light, temperature, oxygen, and humidity - to direct adaptive growth. We detail the molecular mechanisms, such as photoreceptor-mediated activation, thermal resilience pathways, hypoxia sensing, hydraulic dynamics, and mechanical signalling, that regulate stem cell activity. Furthermore, we explore how these environmental cues couple with developmental programs to fine-tune meristem function and organogenesis. By drawing parallels to the environmental regulation of root meristem development, we highlight conserved sensing and signalling modules within meristematic tissues that influence plant growth plasticity. Examining this interplay both in shoot and in root meristems, from evolutionary and applied perspectives, underscores how environmental responsiveness of stem cell niches regulates plant adaptation, informing strategies for engineering climate-resilient crops.
Heterostyly is a classic Darwinian adaptation promoting disassortative pollination. The polymorphism usually depends on floral tubes to enforce spatial segregation of pollen deposited on pollinators. How this is achieved in species with bowl-shaped flowers and generalised pollinators remains less well-understood. We investigated the mechanistic basis of Darwin's cross-promotion hypothesis in distylous Persicaria jucunda, which lacks a floral tube and is fly-pollinated. We integrated morphological measurements of flowers and flies with high-definition video analysis of foraging behaviour. Exploiting pollen-size dimorphism, we quantified morph-specific pollen placement on pollinator body parts and the composition of naturally pollinated stigmatic pollen loads. A 'morphological fit' was evident with fly proboscis length matching lower-level sex organs and upper-level organs matching the position of the head. This morphological congruence caused L-morph pollen to be deposited primarily on proboscides (76.6%) and S-morph pollen on heads (85.7%), resulting in a significantly higher proficiency of intermorph than intramorph pollen transfer. Despite the absence of a floral tube in P. jucunda, our findings of a morphological fit between flower and pollinator structures and consistent foraging behaviour by flies provide mechanistic support for Darwin's cross-promotion hypothesis and resolve the puzzle of how disassortative pollination occurs in open-flowered heterostylous systems.
The summer of 2022 was characterized by compound soil and atmospheric drought (CSAD; low soil water content, SWC, and high vapor pressure deficit, VPD) in Central Europe, threatening forest carbon sequestration and water balance, yet linked ecosystem- and tree-level hydraulic responses remain poorly resolved. We assessed the response and recovery of water relations of a beech-dominated montane mixed deciduous forest in Switzerland (CH-Lae) to the 2022 CSAD through a series of ecosystem-scale (evapotranspiration, ET; canopy conductance, Gs) as well as tree-scale measurements, including leaf-level (leaf water potential, LWP; stomatal conductance, gs), stem-level (nighttime stem rehydration, NSR) and root-level (root water uptake depth, RWU depth) variables. During peak CSAD, ET and Gs declined by up to 50%, driven primarily by low SWC. Midday and predawn LWP declined significantly. Beech and maple accessed deeper water (> 70 cm), maintaining NSR and gs during CSAD and fully recovering thereafter; spruce and fir relied on shallow water (< 30 cm), showing stronger NSR reductions but still full recovery post-CSAD. Our findings demonstrate that species-specific hydraulic traits drive forest-scale water dynamics under CSAD conditions. Integrating these insights into forest adaptation strategies will be critical for sustaining forests under intensifying compound droughts in the future.
Leaf rust, caused by Puccinia hordei, is a major barley disease worldwide. Despite repeated shifts in virulence, contrasting reproductive histories, and emerging fungicide insensitivity, the genomic basis of its diversification and adaptation remains poorly understood. In this study, we generated haplotype-resolved, chromosome-level genome assemblies for two isolates with contrasting virulence and analyzed 41 Australian isolates collected over 54 yr (1966-2020), integrating comparative and population genomics, mating-type gene phylogenies, chromosome-specific k-mer profiling, genome-wide copy-number variation (CNV) analysis, and gene-expression analysis. We identified a structurally dynamic chromosome characterized by repeat-associated rearrangements, structural variation, and lineage-associated CNV, representing the first evidence in a rust fungus of chromosome-scale structural diversification of this extent. Population analyses distinguished clonally expanded lineages from recombination-associated lineages, with mating-type gene phylogenies providing further support for lineage differentiation. More recently collected isolates showed increased duplication-associated variation, and CNV boundaries were associated with structural-variant breakpoints. We also identified lineage-associated amplification of Cyp51, with increased copy number associated with higher transcript abundance, supporting a potential role in fungicide adaptation. Overall, our findings highlight structural variation, contrasting reproductive histories, and lineage-associated CNV as important contributors to diversification in P. hordei, providing insights for future rust pathogen surveillance and management strategies.
Phytophthora root rot, caused by Phytophthora sojae, is a devastating soilborne disease of soybean (Glycine max). However, the epigenetic regulation of soybean responses to P. sojae remains incompletely understood. Here, using genetic, molecular and biochemical approaches, we characterized the functions of LIKE HETEROCHROMATIN PROTEIN 1 (GmLHP1) and its downstream regulatory network. We demonstrated that GmLHP1, as a reader of H3K27me3, negatively regulates soybean resistance to P. sojae. GmLHP1 binds to H3K27me3 peptides in vitro and colocalizes with H3K27me3 marks genome-wide in vivo. The integrated chromatin immunoprecipitation sequencing and RNA sequencing analysis identified the ethylene biosynthesis pathway gene 1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 18 (GmACS18) as being enriched for H3K27me3 and bound by GmLHP1, leading to its transcriptional downregulation. Notably, GmLHP1 associates with the GmACS18 promoter by directly binding to AATTAA motifs and recognizing H3K27me3 marks. Moreover, GmACS18 enhances defense against P. sojae by accumulating the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). Further analysis unveiled that recognition of H3K27me3 by GmLHP1 is essential for regulating soybean resistance to P. sojae through repressing GmACS18 transcription and decreasing ACC accumulation. Our findings reveal a novel epigenetic regulatory mechanism in which the H3K27me3 reader GmLHP1 blocks soybean resistance to P. sojae by repressing ethylene precursor ACC accumulation.
The flowering plant clade Caryophyllales includes many succulent species that grow in drought conditions. Many Caryophyllales species also have betalain pigmentation and medullary bundles, both of which have been linked to stress tolerance, albeit with less precise functional characterisation. We investigated the relationship between the evolution of these traits and drought tolerance in Caryophyllales. We estimated divergence times for Caryophyllales using transcriptomic data; a 50-character morphological matrix based on a comprehensive review of Caryophyllales fossils; a species-level molecular dataset incorporating > 4400 species; and a tip-dating approach. This enabled us to analyse the evolution of drought tolerance, succulence, betalain pigmentation, and medullary bundles. We demonstrate that betalain-pigmented lineages primarily experience drought conditions, with betalains appearing to evolve repeatedly in response to drought during the early evolution of Caryophyllales. We also show that the evolution of succulence and medullary bundles is favoured in betalain-pigmented lineages. However, medullary bundles, unlike succulence, do not show a clear relationship with drought conditions. The evolution of betalains is likely to have enabled Caryophyllales to adapt to and survive stressful conditions, including drought. This may have increased the adaptive advantages of succulence, as its extensive costs are likely offset by its benefits in drought conditions.
Methane (CH4) produced in flooded paddy soils is emitted by passive diffusion, by ebullition and by diffusion through the rice (Oryza sativa) plant. Counter-diffusing oxygen (O2) via shoot to root and rhizosphere will inhibit methanogenesis and support aerobic rhizospheric methanotrophs and heterotrophs. In this study, we analyzed the anatomical, morphological and physiological traits of roots of several rice varieties and used modeling approaches to assess the potential effects on methane emissions. Modeling showed that traits that enhance internal O2 diffusion: increased cortical porosity, a reduced stelar radius, lower respiratory O2 demand and subapical exodermal barriers to radial O2 loss should widen the oxygenated rhizospheres in apical regions and reduce CH4 emissions. This reduction arises because of increased rhizosphere resistance to CH4 diffusion as the methanogenic front retreats rather than increased methanotrophic CH4 consumption. Increasing methanotrophic rate per unit volume raised emissions by narrowing the oxygenated rhizosphere. Larger root radii (with stelar radius constant) increased oxygenated rhizosphere thickness and CH4 consumption, but resistance to CH4 diffusion was sufficiently reduced for CH4 emissions to increase. Overall, the results challenge the widely held assumption that increased methanotrophy will inevitably reduce CH4 emissions. However, increased methanotrophy could reduce emissions where it replaces heterotrophic O2 consumption.
When fungi are seen fruiting on tree trunks, branches and twigs, they are often automatically thought to be causing disease. Likewise, the hollowing of dead woody tissue in the centre of trunks is often instantly thought of as harmful. Yet there is a wide diversity of tree-fungus interactions, and the majority of those involving wood decay fungi do not have negative consequences for the tree. This biologically inaccurate framing of wood decay fungi in general, and heart-rot in particular, has major consequences for research priorities, forest management, and public perceptions of fungi-tree interactions. Heart-rot has important ecological functions, to the extent that research to accelerate heart-rot is ongoing. We must actively reframe the narrative more precisely to represent the actual role of heart-rot as a functional component of tree and forest systems because the logical consequence of describing heart-rot as disease is that valuable trees and the species they support will be lost.
In plants, the epigenetic phenomenon of parent-of-origin allele-specific expression occurs mainly in the triploid endosperm. Although well studied in inbreeding Arabidopsis thaliana, genomic imprinting has been less investigated in outcrossers. In order to investigate a wider role of parental-specific allelic expression, we have analyzed imprinting in whole seeds of the obligate outbreeder Arabidopsis arenosa. High-throughput analysis of imprinting in outbreeding species is hampered by the lack of reference genomes and available sequenced accessions. High degree of allelic variation in outbreeding species may also limit the analysis to loci with less variation. We developed a reference-independent pipeline to detect parental-specific reads. Using different accessions in reciprocal crosses, we detected more than 70 paternally biased imprinted genes and > 500 maternally biased genes. Paternally biased genes showed major enrichment for proteins with ubiquitin protein transferase and ligase activity. Maternally biased genes were enriched for protein pathways directly counteracting paternally enriched genes. Here, we demonstrate an alignment-free protocol to identify imprinted genes that may be successfully applied for imprinting studies in other highly heterozygous outcrossing species. Our results suggest a unique role of genomic imprinting affecting post-transcriptional gene regulation in outbreeding A. arenosa.
Lateral rooting confers essential plasticity to root system architecture, ensuring efficient growth and stress adaptations. Auxin has long been associated with lateral root development, but the intricate regulatory mechanism remains elusive. Here, we show that ABI3, a B3-domain transcription factor, controls lateral root formation by intercepting auxin response in Arabidopsis thaliana. ABI3 deletion promotes lateral rooting, characterised by higher primordia number, density, accelerated emergence and enhanced auxin response, compared to wild-type. While optimum auxin is known to promote lateral rooting, excess auxin inhibits it. We show that auxin concentrations that impair lateral root development augment ABI3 expression. Transactivation assay and ChIP-based results indicate that the auxin-responsive factor ARF19 weakly induces ABI3 expression, probably as part of a secondary auxin response, coupled with ABI3-mediated autoactivation, resulting in higher transcriptional output. ABI3 functions as a transcriptional repressor of MYC2. MYC2 affects auxin biosynthesis and signalling through ERF109 and ASA1, followed by the downstream module of ARF7/19-LBD29, to ensure efficient lateral root development. ABI3-mediated repression of MYC2 acts to attenuate this pathway, restricting lateral root formation. Absence of ABI3 thus augments auxin signalling through MYC2, effectively promoting enhanced lateral root proliferation. ABI3, therefore, functions as a critical regulator that fine-tunes auxin signalling to balance lateral root growth.
RNA interference (RNAi) shows great potential to protect crops against fungal diseases, yet reported protection efficiencies vary greatly, and our understanding of the factors responsible for this variance remains limited. In this meta-analysis, we evaluated 89 studies that compare the efficiency of host-induced gene silencing (HIGS) and spray-induced gene silencing (SIGS) in controlling fungal diseases, focusing on biotrophic, hemibiotrophic, and necrotrophic fungi, the use of formulations, and the dsRNA design as explanatory factors for differences between reported efficiency values. Our results indicate that SIGS is slightly more effective, particularly against biotrophs. Surprisingly, SIGS studies using formulations did not outperform those applying naked dsRNA. We also assessed parameters of RNA design. Differences in dsRNA length and the number of constructs and number of targets showed no consistent significant effect on resistance in either HIGS or SIGS. However, HIGS studies reported significantly higher efficiency when targeting genes closer to the 3' end and SIGS when targeting genes closer to the 5' end. We discuss potential reasons for the reported patterns, such as variability in dsRNA uptake mechanisms, intercellular trafficking, and Dicer processing, and conclude that more research is needed to understand the biological mechanisms determining RNAi efficiency for fungal control.
Microbial-based approaches offer a promising strategy to decrease the use of chemical fertilizers in agriculture. Among them, arbuscular mycorrhizal fungi (AMF), which extend root surface area and enhance phosphate uptake, and phosphate-solubilizing bacteria (PSB) are particularly relevant. However, their effectiveness depends strongly on plant genetic diversity. To identify genetic markers underlying plant responses to beneficial soil microbes, we studied a panel of 128 fully sequenced Lactuca sativa varieties under controlled phosphate-starvation conditions and treated with AMF and PSB. Lettuce genetic variation showed a strong effect on physiological and morphological responses to microbial inoculation. Genome-wide association studies identified specific genomic regions associated with changes in leaf phosphate content and shoot biomass following treatment. Beyond genetic factors, we observed shifts in fungal β-diversity and increased bacterial α-diversity associated with phenotypic variation. We also identified 44 amplicon sequence variants associated with agriculturally relevant traits. Among these, six bacterial strains were experimentally validated through in vitro and pot experiments for their effects on leaf phosphate concentration and shoot biomass. Overall, we highlighted key genetic, microbial, and physiological mechanisms that may enhance microbial treatments for improved plant phosphate management in lettuce.
Whether a widespread bacterial strain of Paraburkholderia can enhance the physiological responses of ectomycorrhizal fungi (EcMF) and host Bishop pine seedling growth remains unclear. We developed a 'top-down meets bottom-up' approach that harmonized data from molecular field surveys, experimental forest soil manipulations, statistical interaction models, metabolomics studies, bacterial isolations, controlled growth chamber experiments, and comparative genomics analyses to test the direction and strength of Paraburkholderia-EcMF interactions on host seedling physiology and identify potential mechanisms that support these tripartite interactions. Paraburkholderia sp. D1E increased host root colonization of Suillus pungens - a keystone EcMF taxon for seedling establishment. Paraburkholderia-Suillus co-inoculations also often drove additive seedling growth responses (e.g. biomass and foliar chemistry) and generated nonadditive, positive effects on seedling shoot height. Genomic comparisons identified low chitin and high arabinitol utilization potential as distinguishing features of Paraburkholderia-EcMF symbioses. Our analyses provide experimental evidence, genomic resources, and cross-data validation that highlight potential mechanisms involved in a widespread bacteria-EcMF-tree interaction. Given the diversity of bacteria and fungi in the rhizosphere, however, this approach should continue to be applied to other species combinations to generalize interaction mechanisms among bacterial, fungal, and plant partners.
Postural control in plant shoots relies on gravi- and photo- tropisms, driven by angular sensing and actuated by differential growth or reaction wood formation (tension wood in dicots). Control theory and kinematical models predict that posture stabilization additionally requires active counter-curving. This led to the hypothesis that plants actively straighten through proprioception (curvature sensing) driving autotropic actuation. However, passive springback can be involved, especially in woody stems, and direct conclusive experimental evidence for proprioception-driven autotropism has been lacking. To assess this hypothesis, we designed a novel experimental setup, allowing us to suspend phototropic and gravitropic sensing on demand along the tropic movement. We then quantified stem movement and tension wood formation - an indicator of actuation - during curving and counter-curving in poplar stems (Populus tremula × alba). We show that counter-curving results from active tension wood formation on the convex side of curved stems until straightness is recovered. Quantitative analysis revealed the curvature-dependent control law governing this response and allowed estimation of proprioceptive sensitivity. Our results establish that reaction wood formation is driven by the balance between graviperceptive and proprioceptive feedbacks, revising our textbook view of tension wood formation. They provide direct evidence that proprioception-driven autotropism is the key process for active straightening in trees.
Phosphorus (P) is a key and often scarce element for the growth and regeneration of trees. Formation of diversified roots and collaboration with different mycorrhizal fungi are crucial mechanisms for nutrient acquisition and species coexistence in forest ecosystems. However, how soil P enrichment modifies functional traits and mycorrhizal symbioses of absorptive tree roots remains unclear. We conducted a comprehensive meta-analysis of 601 observations from 108 studies to assess how fine root morphological, chemical, mycorrhizal, and enzymatic traits respond to soil P addition. We revealed that fine root length was generally promoted and mycorrhizal colonization reduced by P addition, with both effects intensifying along a gradient of P additions. P addition promoted root P concentration for both arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) trees, indicating an overall improvement in plant P status. However, AM trees showed stronger increases in root length, whereas ECM trees showed stronger increases in mycorrhizal fungal biomass. Our findings highlight the significant changes in fine root traits in response to soil P enrichment exhibited by AM and ECM trees, which may lead to different growth strategies between the two main mycorrhizal types and may contribute significantly to ecological niche partitioning and species coexistence under heterogeneous nutrient conditions.
Drought stress disrupts cellular homeostasis and severely limits plant growth. Although proline accumulation is a major adaptive response to water deficit, how drought-responsive regulatory networks control proline biosynthesis in woody grasses remains poorly understood. Here, we combined genetic manipulation, molecular assays, and physiological analyses to investigate the function of the DlamiR156-DlaSPL60 module in Ma bamboo (Dendrocalamus latiflorus Munro). We show that DlamiR156 acts as a negative regulator of drought tolerance by repressing DlaSPL60 via transcript cleavage, whereas drought-induced reduction of DlamiR156 releases this repression; DlaSPL60 directly binds to the DlaP5CS1 promoter and activates its transcription, thereby promoting proline accumulation. Our findings establish a mechanistic link between the conserved miR156-squamosa promoter-binding protein-like regulatory module and proline biosynthesis in bamboo, providing new insights into how post-transcriptional regulation coordinates metabolic reprogramming during drought adaptation in perennial woody grasses.
Root hydraulic conductance (Kr) normalised by root dry mass (including nodules) under hydrated and drought conditions in Pisum sativum wild-type (Frisson, Nod+), non-nodulator (sym19, Nod-), and supernodulator (Psrdn1, Nod++).
WD40 is a highly conserved protein domain in eukaryotes that functions as a versatile platform for protein-protein interactions and participates in diverse biological processes. We performed a genome-wide functional analysis of WD40 domain-containing proteins in Fusarium graminearum, a phytopathogenic fungus that causes severe yield losses and mycotoxin contamination in major cereal crops. Comprehensive phenotypic profiling of 119 WD40 gene deletion mutants across 22 phenotypic traits established a systematic WD40 phenome dataset, revealing the broad functional involvement of WD40 proteins and a strong correlation between sexual reproduction and virulence. Protein interaction analyses of selected WD40 proteins revealed diverse WD40-mediated interaction patterns and provided further insights into WD40-mediated protein interactions and their roles in protein complex formation. This study provides a foundation for further characterization of WD40 proteins in filamentous fungi.
Ceratostigma willmottianum, which can mineralize atmospheric CO2 directly into CaCO3 for long-lasting C sequestration, has both organic and inorganic C sequestration functions. However, how elevated CO2 affects CaCO3 mineralization and the allocation of C between the two C sequestration remains unclear. Therefore, C. willmottianum was exposed to five CO2 concentrations (400, 550, 700, 850, and 1000 ppm) in combination with 13C isotope labeling, carbonic anhydrase (CA) inhibitor treatments, and transient overexpression assays to systematically investigate these effects. Results showed that 700 ppm CO2 was the most effective in promoting plant growth, photosynthesis, and CaCO3 accumulation, whereas 1000 ppm CO2 exerted an inhibitory effect. 13C tracing revealed that elevated CO2 increased C allocation to CaCO3 mineralization from 3.03% (400 ppm) to 4.62% (700 ppm), while decreasing that to net organic C fixation from 63.40 to 60.51%. CA inhibitor experiments further indicated that extracellular CA plays a key role in promoting more C allocation to CaCO3 mineralization. Gene expression and functional validation identified CwβCA2 as a key gene responding to elevated CO2 and promoting CaCO3 mineralization. This study provides a theoretical basis and candidate gene resources for developing biomineralization-based C capture and storage technologies to cope with rising CO2 in the future.
