O Gaju, K J Bloomfield, A C A Negrini, A F Bowerman, D Cullerne, B C Posch, C Bryant, Y Fan, M Spence, B Stone, M Gilliham, R T Furbank, G Molero, B J Pogson, K Mathews, A H Millar, A L Pearson, M P Reynolds, E Stroeher, N L Taylor, M H Turnbull, O K Atkin
{"title":"Accounting for the impact of genotype and environment on variation in leaf respiration of wheat in Mexico and Australia.","authors":"O Gaju, K J Bloomfield, A C A Negrini, A F Bowerman, D Cullerne, B C Posch, C Bryant, Y Fan, M Spence, B Stone, M Gilliham, R T Furbank, G Molero, B J Pogson, K Mathews, A H Millar, A L Pearson, M P Reynolds, E Stroeher, N L Taylor, M H Turnbull, O K Atkin","doi":"10.1093/jxb/erae449","DOIUrl":"https://doi.org/10.1093/jxb/erae449","url":null,"abstract":"<p><p>An approach to improving radiation use efficiency (RUE) in wheat is to screen for variability in rates of leaf respiration in darkness (Rdark). We used a high-throughput system to quantify variation in Rdark among a diverse range of spring wheat genotypes (301 lines) grown in two countries (Mexico and Australia) and two seasons (2017 and 2018), and in doing so quantify the relative importance of genotype (G) and environment (E) in influencing variations in leaf Rdark. Through careful design, residual (unexplained) variation represented less than 10% of the total observed. Up to a third of the variation in Rdark (and related traits) was under genetic control. This suggests opportunities for breeders to use Rdark as a novel selection tool. In addition, E accounted for more than half of the total variation in area-based rates of Rdark. Here, the day of measurement was crucial, suggesting that day-to-day variations in the environment influence rates of Rdark measured at a common temperature. Overall, this study provides new insights into the role G and E play in determining variation in rates of leaf Rdark of one of the most important cereal crops, with implications for future improvements in carbon use efficiency and yield.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":""},"PeriodicalIF":5.6,"publicationDate":"2024-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142644055","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Scott A M McAdam, Anju Manandhar, Cade N Kane, Joel A Mercado-Reyes
{"title":"Passive stomatal closure under extreme drought in an angiosperm species.","authors":"Scott A M McAdam, Anju Manandhar, Cade N Kane, Joel A Mercado-Reyes","doi":"10.1093/jxb/erad510","DOIUrl":"10.1093/jxb/erad510","url":null,"abstract":"<p><p>The phytohormone abscisic acid (ABA) plays a major role in closing the stomata of angiosperms. However, recent reports of some angiosperm species having a peaking-type ABA dynamic, in which under extreme drought ABA levels decline to pre-stressed levels, raises the possibility that passive stomatal closure by leaf water status alone can occur in species from this lineage. To test this hypothesis, we conducted instantaneous rehydration experiments in the peaking-type species Umbellularia californica through a long-term drought, in which ABA levels declined to pre-stress levels, yet stomata remain closed. We found that when ABA levels were lowest during extreme drought, stomata reopen rapidly to maximum rates of gas exchange on instantaneous rehydration, suggesting that the stomata of U. californica were passively closed by leaf water status alone. This contrasts with leaves early in drought, in which ABA levels were highest and stomata did not reopen on instantaneous rehydration. The transition from ABA-driven stomatal closure to passively driven stomatal closure as drought progresses in this species occurs at very low water potentials facilitated by highly embolism-resistant xylem. These results have important implications for understanding stomatal control during drought in angiosperms.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6850-6855"},"PeriodicalIF":8.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139058409","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yazen Al-Salman, Francisco Javier Cano, Emma Mace, David Jordan, Michael Groszmann, Oula Ghannoum
{"title":"High water use efficiency due to maintenance of photosynthetic capacity in sorghum under water stress.","authors":"Yazen Al-Salman, Francisco Javier Cano, Emma Mace, David Jordan, Michael Groszmann, Oula Ghannoum","doi":"10.1093/jxb/erae418","DOIUrl":"10.1093/jxb/erae418","url":null,"abstract":"<p><p>Environmental change requires more crop production per water use to meet the rising global food demands. However, improving crop intrinsic water use efficiency (iWUE) usually comes at the expense of carbon assimilation. Sorghum is a key crop in many vulnerable agricultural systems with higher tolerance to water stress (WS) than most widely planted crops. To investigate physiological controls on iWUE and its inheritance in sorghum, we screened 89 genotypes selected based on inherited haplotypes from an elite line or five exotics lines, containing a mix of geographical origins and dry versus milder climates, which included different aquaporin (AQP) alleles. We found significant variation among key highly heritable gas exchange and hydraulic traits, with some being significantly affected by variation in haplotypes among parental lines. Plants with a higher proportion of the non-stomatal component of iWUE still maintained iWUE under WS by maintaining photosynthetic capacity, independently of reduction in leaf hydraulic conductance. Haplotypes associated with two AQPs (SbPIP1.1 and SbTIP3.2) influenced iWUE and related traits. These findings expand the range of traits that bridge the trade-off between iWUE and productivity in C4 crops, and provide possible genetic regions that can be targeted for breeding.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6778-6795"},"PeriodicalIF":5.6,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11565205/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142390989","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Grace D Tan, Ushasi Chaudhuri, Sebastian Varela, Narendra Ahuja, Andrew D B Leakey
{"title":"Machine learning-enabled computer vision for plant phenotyping: a primer on AI/ML and a case study on stomatal patterning.","authors":"Grace D Tan, Ushasi Chaudhuri, Sebastian Varela, Narendra Ahuja, Andrew D B Leakey","doi":"10.1093/jxb/erae395","DOIUrl":"10.1093/jxb/erae395","url":null,"abstract":"<p><p>Artificial intelligence and machine learning (AI/ML) can be used to automatically analyze large image datasets. One valuable application of this approach is estimation of plant trait data contained within images. Here we review 39 papers that describe the development and/or application of such models for estimation of stomatal traits from epidermal micrographs. In doing so, we hope to provide plant biologists with a foundational understanding of AI/ML and summarize the current capabilities and limitations of published tools. While most models show human-level performance for stomatal density (SD) quantification at superhuman speed, they are often likely to be limited in how broadly they can be applied across phenotypic diversity associated with genetic, environmental, or developmental variation. Other models can make predictions across greater phenotypic diversity and/or additional stomatal/epidermal traits, but require significantly greater time investment to generate ground-truth data. We discuss the challenges and opportunities presented by AI/ML-enabled computer vision analysis, and make recommendations for future work to advance accelerated stomatal phenotyping.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6683-6703"},"PeriodicalIF":5.6,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11565210/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142372033","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Ethylene-mediated stomatal responses to dehydration and rehydration in seed plants.","authors":"Md Mahadi Hasan, Xu-Dong Liu, Guang-Qian Yao, Jianquan Liu, Xiang-Wen Fang","doi":"10.1093/jxb/erae060","DOIUrl":"10.1093/jxb/erae060","url":null,"abstract":"<p><p>Ethylene, a plant hormone that significantly influences both plant growth and response to stress, plays a well-established role in stress signaling. However, its impact on stomatal opening and closure during dehydration and rehydration remains relatively unexplored and is still debated. Exogenous ethylene has been proven to induce stomatal closure through a series of signaling pathways, including the accumulation of reactive oxygen species, subsequent synthesis of nitric oxide and hydrogen sulfide, and SLOW ANION CHANNEL-ASSOCIATED 1 activation. Thus, it has been suggested that ethylene might function to induce stomatal closure synergistically with abscisic acid (ABA). Furthermore, it has also been shown that increased ethylene can inhibit ABA- and jasmonic acid-induced stomatal closure, thus hindering drought-induced closure during dehydration. Simultaneously, other stresses, such as chilling, ozone pollution, and K+ deficiency, inhibit drought- and ABA-induced stomatal closure in an ethylene synthesis-dependent manner. However, ethylene has been shown to take on an opposing role during rehydration, preventing stomatal opening in the absence of ABA through its own signaling pathway. These findings offer novel insights into the function of ethylene in stomatal regulation during dehydration and rehydration, giving a better understanding of the mechanisms underlying ethylene-induced stomatal movement in seed plants.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6719-6732"},"PeriodicalIF":8.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139898040","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ashley Baldwin, Tamara Lechon, Angela Marchbank, Simon Scofield, Kerstin Lieu, Charlotte L Wilson, Richard A Ludlow, Robert J Herbert, Hans-Wilhelm Nützmann, Hilary J Rogers
{"title":"The H3K27me3 histone mark correlates with repression of colour and aroma development post-harvest in strawberry fruit.","authors":"Ashley Baldwin, Tamara Lechon, Angela Marchbank, Simon Scofield, Kerstin Lieu, Charlotte L Wilson, Richard A Ludlow, Robert J Herbert, Hans-Wilhelm Nützmann, Hilary J Rogers","doi":"10.1093/jxb/erae464","DOIUrl":"https://doi.org/10.1093/jxb/erae464","url":null,"abstract":"<p><p>Strawberry ripening is non-climacteric, and post-harvest fruit enter senescence and deteriorate rapidly. Chilled storage induces transcriptome wide changes in gene expression, including the down-regulation of aroma related genes. Histone marks are associated with transcriptional activation or repression; the H3K27me3 mark is mainly associated with repression of gene expression. Here genes associated with H3K27me3 were identified through ChIP-seq in ripe red strawberry fruit at harvest and after 5 days of chilled storage in the dark. The number of ChIP peaks increased with storage time, indicating an increased role for this mark in regulation of gene expression following chilled dark storage. Comparing ChIP-seq data to RNA-seq data from the same material identified 440 genes whose expression correlates with H3K27me3 repression. Abiotic stress genes, especially cold stress response genes, were down-regulated during storage. Increased association with the H3K27me3 mark indicates that they may be repressed via this epigenetic mark. Other functional groups included cell wall and carbohydrate metabolism. The association with the H3K27me3 mark of two transcription factors (FaHY5 and FaTRAB1) and FaADH, involved in ester biosynthesis, was validated by ChIP-PCR. These three genes are all down-regulated during storage and indicate a network of H3K27me3 gene repression affecting both anthocyanin and ester biosynthesis.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":""},"PeriodicalIF":5.6,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142639005","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Application of deep learning for the analysis of stomata: a review of current methods and future directions.","authors":"Jonathon A Gibbs, Alexandra J Burgess","doi":"10.1093/jxb/erae207","DOIUrl":"10.1093/jxb/erae207","url":null,"abstract":"<p><p>Plant physiology and metabolism rely on the function of stomata, structures on the surface of above-ground organs that facilitate the exchange of gases with the atmosphere. The morphology of the guard cells and corresponding pore that make up the stomata, as well as the density (number per unit area), are critical in determining overall gas exchange capacity. These characteristics can be quantified visually from images captured using microscopy, traditionally relying on time-consuming manual analysis. However, deep learning (DL) models provide a promising route to increase the throughput and accuracy of plant phenotyping tasks, including stomatal analysis. Here we review the published literature on the application of DL for stomatal analysis. We discuss the variation in pipelines used, from data acquisition, pre-processing, DL architecture, and output evaluation to post-processing. We introduce the most common network structures, the plant species that have been studied, and the measurements that have been performed. Through this review, we hope to promote the use of DL methods for plant phenotyping tasks and highlight future requirements to optimize uptake, predominantly focusing on the sharing of datasets and generalization of models as well as the caveats associated with utilizing image data to infer physiological function.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6704-6718"},"PeriodicalIF":8.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11565211/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140876581","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
John N Ferguson, Peter Schmuker, Anna Dmitrieva, Truyen Quach, Tieling Zhang, Zhengxiang Ge, Natalya Nersesian, Shirley J Sato, Tom E Clemente, Andrew D B Leakey
{"title":"Reducing stomatal density by expression of a synthetic epidermal patterning factor increases leaf intrinsic water use efficiency and reduces plant water use in a C4 crop.","authors":"John N Ferguson, Peter Schmuker, Anna Dmitrieva, Truyen Quach, Tieling Zhang, Zhengxiang Ge, Natalya Nersesian, Shirley J Sato, Tom E Clemente, Andrew D B Leakey","doi":"10.1093/jxb/erae289","DOIUrl":"10.1093/jxb/erae289","url":null,"abstract":"<p><p>Enhancing crop water use efficiency (WUE) is a key target trait for climatic resilience and expanding cultivation on marginal lands. Engineering lower stomatal density to reduce stomatal conductance (gs) has improved WUE in multiple C3 crop species. However, reducing gs in C3 species often reduces photosynthetic carbon gain. A different response is expected in C4 plants because they possess specialized anatomy and biochemistry which concentrates CO2 at the site of fixation. This modifies the relationship of photosynthesis (AN) with intracellular CO2 concentration (ci), such that photosynthesis is CO2 saturated and reductions in gs are unlikely to limit AN. To test this hypothesis, genetic strategies were investigated to reduce stomatal density in the C4 crop sorghum. Constitutive expression of a synthetic epidermal patterning factor (EPF) transgenic allele in sorghum led to reduced stomatal densities, reduced gs, reduced plant water use, and avoidance of stress during a period of water deprivation. In addition, moderate reduction in stomatal density did not increase stomatal limitation to AN. However, these positive outcomes were associated with negative pleiotropic effects on reproductive development and photosynthetic capacity. Avoiding pleiotropy by targeting expression of the transgene to specific tissues could provide a pathway to improved agronomic outcomes.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6823-6836"},"PeriodicalIF":8.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11565208/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141633683","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The causal arrows from genotype, environment and management to plant phenotype are double headed.","authors":"Victor O Sadras, Peter T Hayman","doi":"10.1093/jxb/erae455","DOIUrl":"https://doi.org/10.1093/jxb/erae455","url":null,"abstract":"<p><p>Cause-and-effect arrows are drawn from genotype (G), environment (E), and agronomic management (M) to the plant phenotype in crop stands in a useful but incomplete framework that informs research questions, experimental design, statistical analysis, data interpretation, modelling, and breeding and agronomic applications. Here we focus on the overlooked bidirectionality of these arrows. The phenotype-to-genotype arrow includes increased mutation rates in stressed phenotypes, relative to basal rates. From a developmental viewpoint, the phenotype modulates gene expression returning multiple cellular phenotypes with a common genome. The phenotype-to-environment arrow is captured in the process of niche construction, which spans from persistent and global to transient and local. Research on crop rotations recognises the influence of the phenotype on the environment but is divorced of niche construction theory. The phenotype-to-management arrow involves, for example, a diseased crop that may trigger fungicide treatment. Making explicit the bidirectionality of the arrows in the G × E × M framework contributes to narrowing the gap between data-driven technologies and integrative theory and is an invitation to cautiously think of the internal teleonomy of plants in contrast to the view of the phenotype as the passive end of the arrows in the current framework.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":""},"PeriodicalIF":5.6,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142639059","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Joseph D Crawford, Robert J Twohey, Varsha S Pathare, Anthony J Studer, Asaph B Cousins
{"title":"Differences in stomatal sensitivity to CO2 and light influence variation in water use efficiency and leaf carbon isotope composition in two genotypes of the C4 plant Zea mays.","authors":"Joseph D Crawford, Robert J Twohey, Varsha S Pathare, Anthony J Studer, Asaph B Cousins","doi":"10.1093/jxb/erae286","DOIUrl":"10.1093/jxb/erae286","url":null,"abstract":"<p><p>The ratio of net CO2 uptake (Anet) and stomatal conductance (gs) is an intrinsic measurement of leaf water use efficiency (WUEi); however, its measurement can be challenging for large phenotypic screens. Measurements of the leaf carbon isotope composition (δ13Cleaf) may be a scalable tool to approximate WUEi for screening because it in part reflects the competing influences of Anet and gs on the CO2 partial pressure (pCO2) inside the leaf over time. However, in C4 photosynthesis, the CO2-concentrating mechanism complicates the relationship between δ13Cleaf and WUEi. Despite this complicated relationship, several studies have shown genetic variation in δ13Cleaf across C4 plants. Yet there has not been a clear demonstration of if Anet or gs are the causal mechanisms controlling WUEi and δ13Cleaf. Our approach was to characterize leaf photosynthetic traits of two Zea mays recombinant inbred lines (Z007E0067 and Z007E0150) which consistently differ for δ13Cleaf even though they have minimal confounding genetic differences. We demonstrate that these two genotypes contrasted in WUEi driven by differences in the speed of stomatal responses to changes in pCO2 and light that lead to unproductive leaf water loss. These findings provide support that differences in δ13Cleaf in closely related genotypes do reflect greater WUEi and further suggest that differences in stomatal kinetic response to changing environmental conditions is a key target to improve WUEi.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"6748-6761"},"PeriodicalIF":8.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141544919","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}