Nature Plants

Uniform regulation of stomatal closure across temperate tree species to sustain nocturnal turgor and growth
Peters RL, Arend M, Zahnd C, Hoch G, Arndt SK, Cernusak LA, Poyatos R, Zhorzel T and Kahmen A
Water loss and carbon gain are balanced by stomatal control, a trade-off that has allowed trees to survive and thrive under fluctuating environmental conditions. During periods of lower water availability, stomatal closure prevents excess water loss. Various strategies of stomatal control have been found among tree species, but the trigger for this behaviour remains elusive. We found a uniform pre-dawn water potential threshold (-1.2 MPa) for stomatal closure across species, which coincided with stem-growth cessation. Meanwhile, midday water potentials at stomatal closure were more variable across species and stomatal control did not follow species-specific thresholds of hydraulic failure, a commonly adopted theory in plant biology, and often used in predictive water-use modelling. This indicates that nocturnal rehydration, rather than daytime hydraulic safety is an optimization priority for stomatal closure in trees. We suggest that these processes are critical for forecasting the global carbon cycle dynamics.
Future crop breeding needs to consider future soils
Raza S, Pandey BK, Hawkesford MJ, Griffiths S, Bennett MJ and Mooney SJ
Making a new epidermis after abscission
Guerault A and Nawrath C
MYB74 transcription factor guides de novo specification of epidermal cells in the abscission zone of Arabidopsis
Wen X, Lee CW, Kim S, Hwang JU, Choi YH, Han SK, Lee E, Yoon TH, Cha DG, Lee S, Son H, Son J, Jung SH, Lee J, Lim H, Chen H, Kim JK and Kwak JM
The waxy cuticle layer is crucial for plant defence, growth and survival, and is produced by epidermal cells, which were thought to be specified only during embryogenesis. New surface cells are exposed during abscission, by which leaves, fruits, flowers and seeds are shed. Recent work has shown that nonepidermal residuum cells (RECs) can accumulate a protective cuticle layer after abscission, implying the potential de novo specification of epidermal cells by transdifferentiation. However, it remains unknown how this process occurs and what advantage this mechanism may offer over the other surface protection alternative, the wound healing pathways. Here we followed this transdifferentiation process with single-cell RNA sequencing analysis of RECs, showing that nonepidermal RECs transdifferentiate into epidermal cells through three distinct stages. During this vulnerable process, which involves a transient period when the protective layer is not yet formed, stress genes that protect the plant from environmental exposure are expressed before epidermis formation, ultimately facilitating cuticle development. We identify a central role for the transcription factor MYB74 in directing the transdifferentiation. In contrast to alternative protective mechanisms, our results suggest that de novo epidermal specification supports the subsequent growth of fruit at the abscission site. Altogether, we reveal a developmental programme by which plants use a transdifferentiation pathway to protect the plant while promoting growth.
Unequal signalling and biosynthesis in daughter cells
Trösch R
Developmental innovation of inferior ovaries and flower sex orchestrated by KNOX1 in cucurbits
Dong Z, Liu X, Guo X, Liu X, Wang B, Shao W, Tian C, Zheng Y, Yu Q, Zhong L, Sun J, Li S, Xin T, Zhang B, Yang T, Lu H, Rose JKC, Lucas WJ, Xu X, Huang S, Liu H and Yang X
In flowering plants, inferior ovaries are key morphological innovations that evolved multiple times from superior ovaries to protect female parts of the flower. However, the developmental mechanisms underlying inferior ovary formation remain largely unknown. Comparative spatial transcriptome mapping and cell lineage reconstructions in developing floral buds of cucumber and tomato, which have inferior and superior ovaries, respectively, revealed that inferior ovaries develop from accelerated receptacle growth resulting from the continuous activity of meristematic stems cells at the base of the cucumber floral organs. Genetic knockout of a receptacle-specific KNOX1 transcription factor in cucumber caused arrest in receptacle growth and yielded bisexual flowers with superior ovaries similar to those of tomato. Here we provide developmental and mechanistic insights into inferior ovary formation and sex determination in cucurbits.
The future of genome editing in plants
Gilbertson L, Puchta H and Slotkin RK
The future of genome editing in plants differs from how it is used today. For both research and product development, we need to think beyond the creation of simple single-nucleotide polymorphisms and short deletions in genes. We believe that the future of genome editing in plants involves mimicking the natural evolutionary processes that have shaped plant genomes and been the target of artificial selection during crop domestication and improvement. This includes programming large structural variations (insertions, duplications, deletions, inversions and translocations) and controlling plant recombination and endogenous transposable elements that naturally reshape plant genomes. The key is that genome editing will be used to reshape plant genomes in a manner that could have happened naturally, but now these changes can be directed rapidly in the laboratory.
An evolutionary bouquet for roses
Malécot V
Phenotypic and genomic signatures across wild Rosa species open new horizons for modern rose breeding
Cheng B, Zhao K, Zhou M, Bourke PM, Zhou L, Wu S, Sun Y, Geng L, Du W, Yang C, Chen J, Huang R, Tian X, Zhang L, Huang H, Han Y, Pan H, Zhang Q, Luo L and Yu C
The cultivation and domestication of roses reflects cultural exchanges and shifts in aesthetics that have resulted in today's most popular ornamental plant group. However, the narrow genetic foundation of cultivated roses limits their further improvement. Wild Rosa species harbour vast genetic diversity, yet their utilization is impeded by taxonomic confusion. Here we generated a phased and gap-free reference genome of Rosa persica for phylogenetic and population genomic analyses of a large collection of Rosa samples. The robust nuclear and plastid phylogenies support most of the morphology-based traditional taxonomy of Rosa. Population genomic analyses disclosed potential genetic exchanges among sections, indicating the northwest and southwest of China as two independent centres of diversity for Rosa. Analyses of domestication traits provide insights into selection processes related to flower colour, fragrance, double flower and resistance. This study provides a comprehensive understanding of rose domestication and lays a solid foundation for future re-domestication and innovative breeding efforts using wild resources.
The dynamic and diverse nature of parenchyma cells in the Arabidopsis root during secondary growth
Lyu M, Iida H, Eekhout T, Mäkelä M, Muranen S, Ye L, Vatén A, Wybouw B, Wang X, De Rybel B and Mähönen AP
During secondary growth, the vascular cambium produces conductive xylem and phloem cells, while the phellogen (cork cambium) deposits phellem (cork) as the outermost protective barrier. Although most of the secondary tissues are made up of parenchyma cells, which are also produced by both cambia, their diversity and function are poorly understood. Here we combined single-cell RNA sequencing analysis with lineage tracing to recreate developmental trajectories of the cell types in the Arabidopsis root undergoing secondary growth. By analysing 93 reporter lines, we were able to identify 20 different cell types or cell states, many of which have not been described before. We additionally observed distinct transcriptome signatures of parenchyma cells depending on their maturation state and proximity to the conductive cell types. Our data show that both xylem and phloem parenchyma tissues are required for normal formation of conductive tissue cell types. Furthermore, we show that mature phloem parenchyma gradually obtains periderm identity, and this transformation can be accelerated by jasmonate treatment or wounding. Our study thus reveals the diversity of parenchyma cells and their capacity to undergo considerable identity changes during secondary growth.
Growth in internal tissues sculpts plant organs in 3D
Horizontally acquired CSP genes contribute to wheat adaptation and improvement
Wang K, Guo G, Bai S, Ma J, Zhang Z, Xing Z, Wang W, Li H, Liang H, Li Z, Si X, Wang J, Liu Q, Xu W, Yang C, Song RF, Li J, He T, Li J, Zeng X, Liang J, Zhang F, Qiu X, Li Y, Bu T, Liu WC, Zhao Y, Huang J, Zhou Y and Song CP
Although horizontal gene transfer (HGT) often facilitates environmental adaptation of recipient organisms, whether and how they might affect crop evolution and domestication is unclear. Here we show that three genes encoding cold-shock proteins (CSPs) were transferred from bacteria to Triticeae, a tribe of the grass family that includes several major staple crops such as wheat, barley and rye. The acquired CSP genes in wheat (TaCSPs) are functionally conserved in their bacterial homologues by encoding a nucleic acid-binding protein. Experimental evidence indicates that TaCSP genes positively regulate drought response and improve photosynthetic efficiency under water-deficient conditions by directly targeting a type 1 metallothionein gene to increase reactive oxygen species scavenging, which in turn contributed to the geographic expansion of wheat. We identified an elite CSP haplotype in Aegilops tauschii, introduction of which to wheat significantly increased drought tolerance, photosynthetic efficiency and grain yields. These findings not only provide major insights into the role of HGT in crop adaptation and domestication, but also demonstrate that novel microbial genes introduced through HGT offer a stable and naturally optimized resource for transgenic crop breeding and improvement.
RNA mA modification meets plant hormones
Shen L and Yu H
Plant hormones are essential signalling molecules that control and coordinate diverse physiological processes in plant development and adaptation to ever-fluctuating environments. This hormonal regulation of plant development and environmental responses has recently been shown to extensively involve the most widespread RNA modification, N-methyladenosine (mA). Here we discuss the current understanding of the crosstalk between mA and plant hormones, focusing on their reciprocal regulation, where hormonal signals induce mA reprogramming and mA affects hormone biosynthesis and signalling cascades. We also highlight new insights into how mA contributes to the hormonal control of plant development and stress responses. Furthermore, we discuss future prospects for unveiling the regulatory networks that orchestrate epitranscriptome-hormone interactions and harnessing the related knowledge accrued to enhance crop productivity and resilience in changing environments.
Non-canonical plant metabolism
Sweetlove LJ, Ratcliffe RG and Fernie AR
Metabolism is essential for plant growth and has become a major target for crop improvement by enhancing nutrient use efficiency. Metabolic engineering is also the basis for producing high-value plant products such as pharmaceuticals, biofuels and industrial biochemicals. An inherent problem for such engineering endeavours is the tendency to view metabolism as a series of distinct metabolic pathways-glycolysis, the tricarboxylic acid cycle, the Calvin-Benson cycle and so on. While these canonical pathways may represent a dominant or frequently occurring flux mode, systematic analyses of metabolism via computational modelling have emphasized the inherent flexibility of the metabolic network to carry flux distributions that are distinct from the canonical pathways. Recent experimental estimates of metabolic network fluxes using C-labelling approaches have revealed numerous instances in which non-canonical pathways occur under different conditions and in different tissues. In this Review, we bring these non-canonical pathways to the fore, summarizing the evidence for their occurrence and the context in which they operate. We also emphasize the importance of non-canonical pathways for metabolic engineering. We argue that the introduction of a high-flux pathway to a desired metabolic product will, by necessity, require non-canonical supporting fluxes in central metabolism to provide the necessary carbon skeletons, energy and reducing power. We illustrate this using the overproduction of isoprenoids and fatty acids as case studies.
Rapid formation of stable autotetraploid rice from genome-doubled F1 hybrids of japonica-indica subspecies
Han X, Li J, Li G, Zhang Z, Lian T, Zhang B, Luo T, Lv R, Cai X, Lin X, Xu C, Wu Y, Gong L, Wendel JF and Liu B
Theory predicts that in the absence of selection, a newly formed segmental allopolyploid will become 'autopolyploidized' if homoeologous exchanges (HEs) occur freely. Moreover, because selection against meiotic abnormalities is expected to be strong in the initial generations, we anticipate HEs to be uncommon in evolved segmental allopolyploids. Here we analysed the whole-genome composition of 202 phenotypically homogeneous and stable rice tetraploid recombinant inbred lines (TRILs) derived from Oryza sativa subsp. japonica subsp. indica hybridization/whole-genome doubling. We measured functional traits related to growth, development and reproductive fitness, and analysed meiotic chromosomal behaviour of the TRILs. We uncover factors that constrain the genomic composition of the TRILs, including asymmetric parental contribution and exclusive uniparental segment retention. Intriguingly, some TRILs that have high fertility and abiotic stress resilience co-occur with largely stabilized meiosis. Our findings comprise evidence supporting the evolutionary possibility of HE-catalysed 'allo-to-auto' polyploidy transitions in nature, with implications for creating new polyploid crops.
Circular RNAs derived from MIR156D promote rice heading by repressing transcription elongation of pri-miR156d through R-loop formation
Su Y, Yi Y, Ge S, Wang Z, Wei Z, Liu X, Zhang C, Xie Q, Wang H, Qian Y, Yu B and Liu Y
In angiosperms, microRNA156 (miR156) acts as an intrinsic, endogenous developmental timer for the age-dependent transition from the juvenile to the adult phase. However, the mechanisms modulating the age-dependent expression pattern of miR156 are still poorly understood. In this Article, we report that circular RNAs (ciMIR156Ds) derived from pri-miR156d negatively regulate miR156 levels in an aging-dependent manner in rice. The ciMIR156D levels increase as plants age, which is inversely correlated with the changes of pri-miR156d and miR156 abundance. Consistent with this observation, ciMIR156Ds deficiency caused by a spontaneous mutation increases pri-miR156d and miR156 levels, resulting in a delayed heading phenotype, whereas ciMIR156Ds overexpression has opposite effects, demonstrating that ciMIR156Ds are negative regulators of miR156. We further show that ciMIR156Ds form R-loops with MIR156D at the region where they derive in an aging-dependent manner, which reduces the occupancy of DNA-dependent RNA polymerase II at that location and hence impedes pri-miR156d elongation. These findings reveal a mechanism for regulating heading date by refining the aging-dependent expression of miR156.
Mechanical interactions between tissue layers underlie plant morphogenesis
Silveira SR, Collet L, Haque SM, Lapierre L, Bagniewska-Zadworna A, Smith RS, Gosselin FP, Routier-Kierzkowska AL and Kierzkowski D
Differential growth between tissues generates mechanical conflicts influencing organogenesis in plants. Here we use the anther, the male floral reproductive organ, as a model system to understand how cell dynamics and tissue-scale mechanics control 3D morphogenesis of a complex shape. Combining deep live-cell imaging, growth analysis, osmotic treatments, genetics and mechanical modelling, we show that localized expansion of internal cells actively drives anther lobe outgrowth, while the epidermis stretches in response. At later stages, mechanical load is transferred to the sub-epidermal layer (endothecium), contributing to proper organ shape. We propose the concept of 'inflation potential', encapsulating mechanical and anatomical features causing differential growth. Our data emphasize the active mechanical role of inner tissue in controlling both organ shape acquisition and cell dynamics in outer layers.
Plant traits shape global spatiotemporal variations in photosynthetic efficiency
Yan Y, Li B, Dechant B, Xu M, Luo X, Qu S, Miao G, Leng J, Shang R, Shu L, Jiang C, Wang H, Jeong S, Ryu Y and Chen JM
Photosynthetic efficiency (PE) quantifies the fraction of absorbed light used in photochemistry to produce chemical energy during photosynthesis and is essential for understanding ecosystem productivity and the global carbon cycle, particularly under conditions of vegetation stress. However, nearly 60% of the global spatiotemporal variance in terrestrial PE remains unexplained. Here we integrate remote sensing and eco-evolutionary optimality theory to derive key plant traits, alongside explainable machine learning and global eddy covariance observations, to uncover the drivers of daily PE variations. Incorporating plant traits into our model increases the explained daily PE variance from 36% to 80% for C vegetation and from 54% to 84% for C vegetation compared with using climate data alone. Key plant traits-including chlorophyll content, leaf longevity and leaf mass per area-consistently emerge as important factors across global biomes and temporal scales. Water availability and light conditions are also critical in regulating PE, underscoring the need for an integrative approach that combines plant traits with climatic factors. Overall, our findings demonstrate the potential of remote sensing and eco-evolutionary optimality theory to capture principal PE drivers, offering valuable tools for more accurately predicting ecosystem productivity and improving Earth system models under climate change.
Horizontal gene transfer of cold shock protein genes boosted wheat adaptation and expansion
The future of dsRNA-based biopesticides will require global regulatory cohesion
Gunasekara S, Fidelman P, Fletcher S, Gardiner D, Manzie N, Ashworth P, Tardin-Coelho R and Mitter N
H3K36 methylation stamps transcription resistive to preserve development in plants
Yao Y, Zhou J, Wang J, Lei X, Jiang A and Sun Q
Eukaryotic euchromatin is the less-compact chromatin and is modified by many histone modifications such as H3 lysine 36 methylation (H3K36me). Here we report a new chromatin state, 'transcription resistive', which is differentiated from activation and silencing. Transcription resistive is stamped by H3K36me with almost undetectable transcription activity but open-chromatin state, and occupies most documented plant essential genes. Mutating SDG8, previously known as the major H3K36 methyltransferase in Arabidopsis, surprisingly elevates 78.7% of H3K36me3-marked resistive loci, which accounts for 39.4% of the coding genome. Genetically, SDG8 prevents H3K36me activity of SDG4 at short and intronless genes to secure plant fertility, while it collaborates with other H3K36me methyltransferases on long and intron-rich genes. Together, our results reveal that SDG8 is the primary sensor that suppresses excessive H3K36me, and uncovered that 'transcription resistive' is a conserved H3K36me-stamped novel transcription state in plants, highlighting the regulatory diversities and biological significance of H3K36 methylation in eukaryotes.