S1 basic leucine zipper transcription factors shape plant architecture by controlling C/N partitioning to apical and lateral organs.
Kreisz, P., Hellens, A. M., Fröschel, C., Krischke, M., Maag, D., Feil, R., Wildenhain, T., Draken, J., Braune, G., Erdelitsch, L., Cecchino, L., Wagner, T. C., Ache, P., Mueller, M. J., Becker, D., Lunn, J. E., Hanson, J., Beveridge, C. A., Fichtner, F., Barbier, F. F., & Weiste, C.
Proceedings of the National Academy of Sciences, 121(7): e2313343121. February 2024.
Publisher: Proceedings of the National Academy of Sciences
Paper
doi
link
bibtex
abstract
@article{kreisz_s1_2024,
title = {S1 basic leucine zipper transcription factors shape plant architecture by controlling {C}/{N} partitioning to apical and lateral organs},
volume = {121},
url = {https://www.pnas.org/doi/10.1073/pnas.2313343121},
doi = {10.1073/pnas.2313343121},
abstract = {Plants tightly control growth of their lateral organs, which led to the concept of apical dominance. However, outgrowth of the dormant lateral primordia is sensitive to the plant’s nutritional status, resulting in an immense plasticity in plant architecture. While the impact of hormonal regulation on apical dominance is well characterized, the prime importance of sugar signaling to unleash lateral organ formation has just recently emerged. Here, we aimed to identify transcriptional regulators, which control the trade-off between growth of apical versus lateral organs. Making use of locally inducible gain-of-function as well as single and higher-order loss-of-function approaches of the sugar-responsive S1-basic-leucine-zipper (S1-bZIP) transcription factors, we disclosed their largely redundant function in establishing apical growth dominance. Consistently, comprehensive phenotypical and analytical studies of S1-bZIP mutants show a clear shift of sugar and organic nitrogen (N) allocation from apical to lateral organs, coinciding with strong lateral organ outgrowth. Tissue-specific transcriptomics reveal specific clade III SWEET sugar transporters, crucial for long-distance sugar transport to apical sinks and the glutaminase GLUTAMINE AMIDO-TRANSFERASE 1\_2.1, involved in N homeostasis, as direct S1-bZIP targets, linking the architectural and metabolic mutant phenotypes to downstream gene regulation. Based on these results, we propose that S1-bZIPs control carbohydrate (C) partitioning from source leaves to apical organs and tune systemic N supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.},
number = {7},
urldate = {2024-03-18},
journal = {Proceedings of the National Academy of Sciences},
author = {Kreisz, Philipp and Hellens, Alicia M. and Fröschel, Christian and Krischke, Markus and Maag, Daniel and Feil, Regina and Wildenhain, Theresa and Draken, Jan and Braune, Gabriel and Erdelitsch, Leon and Cecchino, Laura and Wagner, Tobias C. and Ache, Peter and Mueller, Martin J. and Becker, Dirk and Lunn, John E. and Hanson, Johannes and Beveridge, Christine A. and Fichtner, Franziska and Barbier, Francois F. and Weiste, Christoph},
month = feb,
year = {2024},
note = {Publisher: Proceedings of the National Academy of Sciences},
pages = {e2313343121},
}
Plants tightly control growth of their lateral organs, which led to the concept of apical dominance. However, outgrowth of the dormant lateral primordia is sensitive to the plant’s nutritional status, resulting in an immense plasticity in plant architecture. While the impact of hormonal regulation on apical dominance is well characterized, the prime importance of sugar signaling to unleash lateral organ formation has just recently emerged. Here, we aimed to identify transcriptional regulators, which control the trade-off between growth of apical versus lateral organs. Making use of locally inducible gain-of-function as well as single and higher-order loss-of-function approaches of the sugar-responsive S1-basic-leucine-zipper (S1-bZIP) transcription factors, we disclosed their largely redundant function in establishing apical growth dominance. Consistently, comprehensive phenotypical and analytical studies of S1-bZIP mutants show a clear shift of sugar and organic nitrogen (N) allocation from apical to lateral organs, coinciding with strong lateral organ outgrowth. Tissue-specific transcriptomics reveal specific clade III SWEET sugar transporters, crucial for long-distance sugar transport to apical sinks and the glutaminase GLUTAMINE AMIDO-TRANSFERASE 1_2.1, involved in N homeostasis, as direct S1-bZIP targets, linking the architectural and metabolic mutant phenotypes to downstream gene regulation. Based on these results, we propose that S1-bZIPs control carbohydrate (C) partitioning from source leaves to apical organs and tune systemic N supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.
Fungal-Bacterial Combinations in Plant Health under Stress: Physiological and Biochemical Characteristics of the Filamentous Fungus Serendipita indica and the Actinobacterium Zhihengliuella sp. ISTPL4 under In Vitro Arsenic Stress.
Sharma, N., Koul, M., Joshi, N. C., Dufossé, L., & Mishra, A.
Microorganisms, 12(2): 405. February 2024.
Number: 2 Publisher: Multidisciplinary Digital Publishing Institute
Paper
doi
link
bibtex
abstract
@article{sharma_fungal-bacterial_2024,
title = {Fungal-{Bacterial} {Combinations} in {Plant} {Health} under {Stress}: {Physiological} and {Biochemical} {Characteristics} of the {Filamentous} {Fungus} {Serendipita} indica and the {Actinobacterium} {Zhihengliuella} sp. {ISTPL4} under {In} {Vitro} {Arsenic} {Stress}},
volume = {12},
copyright = {http://creativecommons.org/licenses/by/3.0/},
issn = {2076-2607},
shorttitle = {Fungal-{Bacterial} {Combinations} in {Plant} {Health} under {Stress}},
url = {https://www.mdpi.com/2076-2607/12/2/405},
doi = {10.3390/microorganisms12020405},
abstract = {Fungal-bacterial combinations have a significant role in increasing and improving plant health under various stress conditions. Metabolites secreted by fungi and bacteria play an important role in this process. Our study emphasizes the significance of secondary metabolites secreted by the fungus Serendipita indica alone and by an actinobacterium Zhihengliuella sp. ISTPL4 under normal growth conditions and arsenic (As) stress condition. Here, we evaluated the arsenic tolerance ability of S. indica alone and in combination with Z. sp. ISTPL4 under in vitro conditions. The growth of S. indica and Z. sp. ISTPL4 was measured in varying concentrations of arsenic and the effect of arsenic on spore size and morphology of S. indica was determined using confocal microscopy and scanning electron microscopy. The metabolomics study indicated that S. indica alone in normal growth conditions and under As stress released pentadecanoic acid, glycerol tricaprylate, L-proline and cyclo(L-prolyl-L-valine). Similarly, d-Ribose, 2-deoxy-bis(thioheptyl)-dithioacetal were secreted by a combination of S. indica and Z. sp. ISTPL4. Confocal studies revealed that spore size of S. indica decreased by 18\% at 1.9 mM and by 15\% when in combination with Z. sp. ISTPL4 at a 2.4 mM concentration of As. Arsenic above this concentration resulted in spore degeneration and hyphae fragmentation. Scanning electron microscopy (SEM) results indicated an increased spore size of S. indica in the presence of Z. sp. ISTPL4 (18 ± 0.75 µm) compared to S. indica alone (14 ± 0.24 µm) under normal growth conditions. Our study concluded that the suggested combination of microbial consortium can be used to increase sustainable agriculture by combating biotic as well as abiotic stress. This is because the metabolites released by the microbial combination display antifungal and antibacterial properties. The metabolites, besides evading stress, also confer other survival strategies. Therefore, the choice of consortia and combination partners is important and can help in developing strategies for coping with As stress.},
language = {en},
number = {2},
urldate = {2024-03-18},
journal = {Microorganisms},
author = {Sharma, Neha and Koul, Monika and Joshi, Naveen Chandra and Dufossé, Laurent and Mishra, Arti},
month = feb,
year = {2024},
note = {Number: 2
Publisher: Multidisciplinary Digital Publishing Institute},
keywords = {\textit{Oryza sativa}, \textit{Serendipita indica}, arsenic, heavy metal stress, secondary metabolites},
pages = {405},
}
Fungal-bacterial combinations have a significant role in increasing and improving plant health under various stress conditions. Metabolites secreted by fungi and bacteria play an important role in this process. Our study emphasizes the significance of secondary metabolites secreted by the fungus Serendipita indica alone and by an actinobacterium Zhihengliuella sp. ISTPL4 under normal growth conditions and arsenic (As) stress condition. Here, we evaluated the arsenic tolerance ability of S. indica alone and in combination with Z. sp. ISTPL4 under in vitro conditions. The growth of S. indica and Z. sp. ISTPL4 was measured in varying concentrations of arsenic and the effect of arsenic on spore size and morphology of S. indica was determined using confocal microscopy and scanning electron microscopy. The metabolomics study indicated that S. indica alone in normal growth conditions and under As stress released pentadecanoic acid, glycerol tricaprylate, L-proline and cyclo(L-prolyl-L-valine). Similarly, d-Ribose, 2-deoxy-bis(thioheptyl)-dithioacetal were secreted by a combination of S. indica and Z. sp. ISTPL4. Confocal studies revealed that spore size of S. indica decreased by 18% at 1.9 mM and by 15% when in combination with Z. sp. ISTPL4 at a 2.4 mM concentration of As. Arsenic above this concentration resulted in spore degeneration and hyphae fragmentation. Scanning electron microscopy (SEM) results indicated an increased spore size of S. indica in the presence of Z. sp. ISTPL4 (18 ± 0.75 µm) compared to S. indica alone (14 ± 0.24 µm) under normal growth conditions. Our study concluded that the suggested combination of microbial consortium can be used to increase sustainable agriculture by combating biotic as well as abiotic stress. This is because the metabolites released by the microbial combination display antifungal and antibacterial properties. The metabolites, besides evading stress, also confer other survival strategies. Therefore, the choice of consortia and combination partners is important and can help in developing strategies for coping with As stress.
Biohybrid Energy Storage Circuits Based on Electronically Functionalized Plant Roots.
Parker, D., Dar, A. M., Armada-Moreira, A., Bernacka Wojcik, I., Rai, R., Mantione, D., & Stavrinidou, E.
ACS Applied Materials & Interfaces. March 2024.
Publisher: American Chemical Society
Paper
doi
link
bibtex
abstract
@article{parker_biohybrid_2024,
title = {Biohybrid {Energy} {Storage} {Circuits} {Based} on {Electronically} {Functionalized} {Plant} {Roots}},
issn = {1944-8244},
url = {https://doi.org/10.1021/acsami.3c16861},
doi = {10.1021/acsami.3c16861},
abstract = {Biohybrid systems based on plants integrate plant structures and processes into technological components targeting more sustainable solutions. Plants’ biocatalytic machinery, for example, has been leveraged for the organization of electronic materials directly in the vasculature and roots of living plants, resulting in biohybrid electrochemical devices. Among other applications, energy storage devices were demonstrated where the charge storage electrodes were seamlessly integrated into the plant tissue. However, the capacitance and the voltage output of a single biohybrid supercapacitor are limited. Here, we developed biohybrid circuits based on functionalized conducting roots, extending the performance of plant based biohybrid energy storage systems. We show that root-supercapacitors can be combined in series and in parallel configuration, achieving up to 1.5 V voltage output or up to 11 mF capacitance, respectively. We further demonstrate that the supercapacitors circuit can be charged with an organic photovoltaic cell, and that the stored charge can be used to power an electrochromic display or a bioelectronic device. Furthermore, the functionalized roots degrade in composting similarly to native roots. The proof-of-concept demonstrations illustrate the potential of this technology to achieve more sustainable solutions for powering low consumption devices such as bioelectronics for agriculture or IoT applications.},
urldate = {2024-03-08},
journal = {ACS Applied Materials \& Interfaces},
author = {Parker, Daniela and Dar, Abdul Manan and Armada-Moreira, Adam and Bernacka Wojcik, Iwona and Rai, Rajat and Mantione, Daniele and Stavrinidou, Eleni},
month = mar,
year = {2024},
note = {Publisher: American Chemical Society},
}
Biohybrid systems based on plants integrate plant structures and processes into technological components targeting more sustainable solutions. Plants’ biocatalytic machinery, for example, has been leveraged for the organization of electronic materials directly in the vasculature and roots of living plants, resulting in biohybrid electrochemical devices. Among other applications, energy storage devices were demonstrated where the charge storage electrodes were seamlessly integrated into the plant tissue. However, the capacitance and the voltage output of a single biohybrid supercapacitor are limited. Here, we developed biohybrid circuits based on functionalized conducting roots, extending the performance of plant based biohybrid energy storage systems. We show that root-supercapacitors can be combined in series and in parallel configuration, achieving up to 1.5 V voltage output or up to 11 mF capacitance, respectively. We further demonstrate that the supercapacitors circuit can be charged with an organic photovoltaic cell, and that the stored charge can be used to power an electrochromic display or a bioelectronic device. Furthermore, the functionalized roots degrade in composting similarly to native roots. The proof-of-concept demonstrations illustrate the potential of this technology to achieve more sustainable solutions for powering low consumption devices such as bioelectronics for agriculture or IoT applications.
A proxitome-RNA-capture approach reveals that processing bodies repress coregulated hub genes.
Liu, C., Mentzelopoulou, A., Hatzianestis, I. H, Tzagkarakis, E., Skaltsogiannis, V., Ma, X., Michalopoulou, V. A, Romero-Campero, F. J, Romero-Losada, A. B, Sarris, P. F, Marhavy, P., Bölter, B., Kanterakis, A., Gutierrez-Beltran, E., & Moschou, P. N
The Plant Cell, 36(3): 559–584. March 2024.
Paper
doi
link
bibtex
abstract
@article{liu_proxitome-rna-capture_2024,
title = {A proxitome-{RNA}-capture approach reveals that processing bodies repress coregulated hub genes},
volume = {36},
issn = {1040-4651},
url = {https://doi.org/10.1093/plcell/koad288},
doi = {10.1093/plcell/koad288},
abstract = {Cellular condensates are usually ribonucleoprotein assemblies with liquid- or solid-like properties. Because these subcellular structures lack a delineating membrane, determining their compositions is difficult. Here we describe a proximity-biotinylation approach for capturing the RNAs of the condensates known as processing bodies (PBs) in Arabidopsis (Arabidopsis thaliana). By combining this approach with RNA detection, in silico, and high-resolution imaging approaches, we studied PBs under normal conditions and heat stress. PBs showed a much more dynamic RNA composition than the total transcriptome. RNAs involved in cell wall development and regeneration, plant hormonal signaling, secondary metabolism/defense, and RNA metabolism were enriched in PBs. RNA-binding proteins and the liquidity of PBs modulated RNA recruitment, while RNAs were frequently recruited together with their encoded proteins. In PBs, RNAs follow distinct fates: in small liquid-like PBs, RNAs get degraded while in more solid-like larger ones, they are stored. PB properties can be regulated by the actin-polymerizing SCAR (suppressor of the cyclic AMP)-WAVE (WASP family verprolin homologous) complex. SCAR/WAVE modulates the shuttling of RNAs between PBs and the translational machinery, thereby adjusting ethylene signaling. In summary, we provide an approach to identify RNAs in condensates that allowed us to reveal a mechanism for regulating RNA fate.},
number = {3},
urldate = {2024-03-01},
journal = {The Plant Cell},
author = {Liu, Chen and Mentzelopoulou, Andriani and Hatzianestis, Ioannis H and Tzagkarakis, Epameinondas and Skaltsogiannis, Vasileios and Ma, Xuemin and Michalopoulou, Vassiliki A and Romero-Campero, Francisco J and Romero-Losada, Ana B and Sarris, Panagiotis F and Marhavy, Peter and Bölter, Bettina and Kanterakis, Alexandros and Gutierrez-Beltran, Emilio and Moschou, Panagiotis N},
month = mar,
year = {2024},
pages = {559--584},
}
Cellular condensates are usually ribonucleoprotein assemblies with liquid- or solid-like properties. Because these subcellular structures lack a delineating membrane, determining their compositions is difficult. Here we describe a proximity-biotinylation approach for capturing the RNAs of the condensates known as processing bodies (PBs) in Arabidopsis (Arabidopsis thaliana). By combining this approach with RNA detection, in silico, and high-resolution imaging approaches, we studied PBs under normal conditions and heat stress. PBs showed a much more dynamic RNA composition than the total transcriptome. RNAs involved in cell wall development and regeneration, plant hormonal signaling, secondary metabolism/defense, and RNA metabolism were enriched in PBs. RNA-binding proteins and the liquidity of PBs modulated RNA recruitment, while RNAs were frequently recruited together with their encoded proteins. In PBs, RNAs follow distinct fates: in small liquid-like PBs, RNAs get degraded while in more solid-like larger ones, they are stored. PB properties can be regulated by the actin-polymerizing SCAR (suppressor of the cyclic AMP)-WAVE (WASP family verprolin homologous) complex. SCAR/WAVE modulates the shuttling of RNAs between PBs and the translational machinery, thereby adjusting ethylene signaling. In summary, we provide an approach to identify RNAs in condensates that allowed us to reveal a mechanism for regulating RNA fate.
High-quality genome assembly enables prediction of allele-specific gene expression in hybrid poplar.
Shi, T., Jia, K., Bao, Y., Nie, S., Tian, X., Yan, X., Chen, Z., Li, Z., Zhao, S., Ma, H., Zhao, Y., Li, X., Zhang, R., Guo, J., Zhao, W., El-Kassaby, Y. A., Müller, N., Van de Peer, Y., Wang, X., Street, N. R., Porth, I., An, X., & Mao, J.
Plant Physiology,kiae078. February 2024.
Paper
doi
link
bibtex
abstract
@article{shi_high-quality_2024,
title = {High-quality genome assembly enables prediction of allele-specific gene expression in hybrid poplar},
issn = {0032-0889},
url = {https://doi.org/10.1093/plphys/kiae078},
doi = {10.1093/plphys/kiae078},
abstract = {Poplar (Populus) is a well-established model system for tree genomics and molecular breeding, and hybrid poplar is widely used in forest plantations. However, distinguishing its diploid homologous chromosomes is difficult, complicating advanced functional studies on specific alleles. In this study, we applied a trio-binning design and PacBio High-Fidelity long-read sequencing to obtain haplotype-phased telomere-to-telomere genome assemblies for the two parents of the well-studied F1 hybrid “84K” (Populus alba × P. tremula var. glandulosa). Almost all chromosomes, including the telomeres and centromeres, were completely assembled for each haplotype subgenome apart from two small gaps on one chromosome. By incorporating information from these haplotype assemblies and extensive RNA-seq data, we analyzed gene expression patterns between the two subgenomes and alleles. Transcription bias at the subgenome level was not uncovered, but extensive expression differences were detected between alleles. We developed machine-learning (ML) models to predict allele-specific expression (ASE) with high accuracy and identified underlying genome features most highly influencing ASE. One of our models with 15 predictor variables achieved 77\% accuracy on the training set and 74\% accuracy on the testing set. ML models identified gene body CHG methylation, sequence divergence, and transposon occupancy both upstream and downstream of alleles as important factors for ASE. Our haplotype-phased genome assemblies and ML strategy highlight an avenue for functional studies in Populus and provide additional tools for studying ASE and heterosis in hybrids.},
urldate = {2024-03-01},
journal = {Plant Physiology},
author = {Shi, Tian-Le and Jia, Kai-Hua and Bao, Yu-Tao and Nie, Shuai and Tian, Xue-Chan and Yan, Xue-Mei and Chen, Zhao-Yang and Li, Zhi-Chao and Zhao, Shi-Wei and Ma, Hai-Yao and Zhao, Ye and Li, Xiang and Zhang, Ren-Gang and Guo, Jing and Zhao, Wei and El-Kassaby, Yousry Aly and Müller, Niels and Van de Peer, Yves and Wang, Xiao-Ru and Street, Nathaniel Robert and Porth, Ilga and An, Xinmin and Mao, Jian-Feng},
month = feb,
year = {2024},
pages = {kiae078},
}
Poplar (Populus) is a well-established model system for tree genomics and molecular breeding, and hybrid poplar is widely used in forest plantations. However, distinguishing its diploid homologous chromosomes is difficult, complicating advanced functional studies on specific alleles. In this study, we applied a trio-binning design and PacBio High-Fidelity long-read sequencing to obtain haplotype-phased telomere-to-telomere genome assemblies for the two parents of the well-studied F1 hybrid “84K” (Populus alba × P. tremula var. glandulosa). Almost all chromosomes, including the telomeres and centromeres, were completely assembled for each haplotype subgenome apart from two small gaps on one chromosome. By incorporating information from these haplotype assemblies and extensive RNA-seq data, we analyzed gene expression patterns between the two subgenomes and alleles. Transcription bias at the subgenome level was not uncovered, but extensive expression differences were detected between alleles. We developed machine-learning (ML) models to predict allele-specific expression (ASE) with high accuracy and identified underlying genome features most highly influencing ASE. One of our models with 15 predictor variables achieved 77% accuracy on the training set and 74% accuracy on the testing set. ML models identified gene body CHG methylation, sequence divergence, and transposon occupancy both upstream and downstream of alleles as important factors for ASE. Our haplotype-phased genome assemblies and ML strategy highlight an avenue for functional studies in Populus and provide additional tools for studying ASE and heterosis in hybrids.