Distinct latitudinal community patterns of Arctic marine vertebrates along the East Greenlandic coast detected by environmental DNA

Aim: Greenland is one of the places on Earth where the effects of climate change are most evident. The retreat of sea ice has made East Greenland more accessible for longer periods during the year. East Greenland fjords have been notoriously difficult to study due to their remoteness, dense sea ice conditions and lack of infrastructure. As a result, biological monitoring across latitudinal gradients is scarce in East Greenland and relies on sporadic research cruises and trawl data from commercial vessels. We here aim to investigate the transition in fish and marine mammal communities from South to Northeast Greenland using environmental DNA (eDNA). Location: South to Northeast Greenland. Methods: We investigated the transition in fish and marine mammal communities from South to Northeast Greenland using eDNA metabarcoding of seawater samples. We included both surface and mesopelagic samples, collected over approximately 2400 km waterway distance, by sampling from Cape Farewell to Ella Island in August 2021. Results: We demonstrate a clear transition in biological communities from south to northeast, with detected fish and mammal species matching known distributions. Samples from the southern areas were dominated by capelin (Mallotus villosus) and redfish (Sebastes), whereas northeastern samples were dominated by polar cod (Boreogadus saida), sculpins (Myoxocephalus) and ringed seal (Pusa hispida). We provide newly generated 12S rRNA barcodes from 87 fish species, bringing the public DNA database closer to full taxonomic coverage for Greenlandic fish species for this locus. Main Conclusions: Our results demonstrate that eDNA sampling can detect latitudinal shifts in marine biological communities of the Arctic region, which can supplement traditional fish surveys in understanding species distributions and community compositions of marine vertebrates. Importantly, sampling of eDNA can be a feasible approach for detecting northward range expansions in remote areas as climate change progresses

Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone

Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors—nitrate (NO3−) or oxygen (O2)—makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3− metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3− storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3− availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3− availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3− is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3− and O2

Biological nitrate transport in sediments on the Peruvian margin mitigates benthic sulfide emissions and drives pelagic N loss during stagnation events

Highlights • Very high rates of dissimilatory nitrate reduction to ammonium by Thioploca. • Non-steady state model predicts Thioploca survival on intracellular nitrate reservoir. • Ammonium release by Thioploca may be coupled to pelagic N loss by anammox. • Thioploca may contribute to anammox long after bottom water nitrate disappearance. • Model indicates that benthic foraminifera account for 90% of benthic N2 production. Abstract Benthic N cycling in the Peruvian oxygen minimum zone (OMZ) was investigated at ten stations along 12oS from the middle shelf (74 m) to the upper slope (1024 m) using in situ flux measurements, sediment biogeochemistry and modelling. Middle shelf sediments were covered by mats of the filamentous bacteria Thioploca spp. and contained a large ‘hidden’ pool of nitrate that was not detectable in the porewater. This was attributed to a biological nitrate reservoir stored within the bacteria to oxidize sulfide to sulfate during ‘dissimilatory nitrate reduction to ammonium’ (DNRA). The extremely high rates of DNRA on the shelf (15.6 mmol m-2 d-1 of N), determined using an empirical steady-state model, could easily supply all the ammonium requirements for anammox in the water column. The model further showed that denitrification by foraminifera may account for 90% of N2 production at the lower edge of the OMZ. At the time of sampling, dissolved oxygen was below detection limit down to 400 m and the water body overlying the shelf had stagnated, resulting in complete depletion of nitrate and nitrite. A decrease in the biological nitrate pool was observed on the shelf during fieldwork concomitant with a rise in porewater sulfide levels in surface sediments to 2 mM. Using a non-steady state model to simulate this natural anoxia experiment, these observations were shown to be consistent with Thioploca surviving on a dwindling intracellular nitrate reservoir to survive the stagnation period. The model shows that sediments hosting Thioploca are able to maintain high ammonium fluxes for many weeks following stagnation, potentially sustaining pelagic N loss by anammox. In contrast, sulfide emissions remain low, reducing the economic risk to the Peruvian fishery by toxic sulfide plume development

Interplay of flg22-induced defence responses and nodulation in Lotus japonicus

In this study the interplay between the symbiotic and defence signalling pathways in Lotus japonicus was investigated by comparing the responses to Mesorhizobium loti, the symbiotic partner of L. japonicus, and the elicitor flg22, a conserved peptide motif present in flagellar protein of a wide range of bacteria. It was found that defence and symbiotic pathways overlap in the interaction between L. japonicus and M. loti since similar responses were induced by the mutualistic bacteria and flg22. However, purified flagellin from M. loti did not induce any response in L. japonicus, which suggests the production of other elicitors by the symbiotic bacteria. Defence responses induced by flg22 caused inhibition of rhizobial infection and delay in nodule organogenesis, as demonstrated by the negative effect of flg22 in the formation of spontaneous nodules in the snf1 L. japonicus mutant, and the inhibition of NSP1 and NSP2 genes. This indicates the antagonistic effect of the defence pathway on the nodule formation in the initial rhizobium–legume interaction. However, the fact that flg22 did not affect the formation of new nodules once the symbiosis was established indicates that after the colonization of the host plant by the symbiotic partner, the symbiotic pathway has prevalence over the defensive response. This result is also supported by the down-regulation of the expression levels of the flg22 receptor FLS2 in the nodular tissue

Impact of intentionally injected carbon dioxide hydrate on deep-sea benthic foraminiferal survival

Author Posting. © The Authors, 2009. This is the author's version of the work. It is posted here by permission of Blackwell for personal use, not for redistribution. The definitive version was published in Global Change Biology 15 (2009): 2078-2088, doi:10.1111/j.1365-2486.2008.01822.x.Sequestration of carbon dioxide (CO2) in the ocean is being considered as a feasible mechanism to mitigate the alarming rate in its atmospheric rise. Little is known, however, about how the resulting hypercapnia and ocean acidification may affect marine fauna. In an effort to understand better the protistan reaction to such an environmental perturbation, the survivorship of benthic foraminifera, which is a prevalent group of protists, was studied in response to deep-sea CO2 release. The survival response of calcareous, agglutinated, and thecate foraminifera was determined in two experiments at ~3.1 and 3.3 km water depth in Monterey Bay (California, USA). Approximately five weeks after initial seafloor CO2 release, in situ incubations of the live-dead indicator CellTracker Green were executed within seafloor-emplaced pushcores. Experimental treatments included direct exposure to CO2 hydrate, two levels of lesser exposure adjacent to CO2 hydrate, and controls, which were far removed from the CO2 hydrate release. Results indicate that survivorship rates of agglutinated and thecate foraminifera were not significantly impacted by direct exposure but the survivorship of calcareous foraminifera was significantly lower in direct exposure treatments compared to controls. Observations suggest that, if large scale CO2 sequestration is enacted on the deep-sea floor, survival of two major groups of this prevalent protistan taxon will likely not be severely impacted, while calcareous foraminifera will face considerable challenges to maintain their benthic populations in areas directly exposed to CO2 hydrate.This work was funded by the Monterey Bay Aquarium Research Institute (project 200002; to JPB), US Department of Energy grant # DE-FG02-03ER63696 (to J. P. Kennett and J.M.B.), and NSF OCE-0725966 (to J.M.B.)

Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development

[EN] The NOOT-BOP-COCH-LIKE (NBCL) genes are orthologs of Arabidopsis thaliana BLADE-ON-PETIOLE1/2. The NBCLs are developmental regulators essential for plant shaping, mainly through the regulation of organ boundaries, the promotion of lateral organ differentiation and the acquisition of organ identity. In addition to their roles in leaf, stipule and flower development, NBCLs are required for maintaining the identity of indeterminate nitrogen-fixing nodules with persistent meristems in legumes. In legumes forming determinate nodules, without persistent meristem, the roles of NBCL genes are not known. We thus investigated the role of Lotus japonicus NOOT-BOP-COCH-LIKE1 (LjNBCL1) in determinate nodule identity and studied its functions in aerial organ development using LORE1 insertional mutants and RNA interference-mediated silencing approaches. In Lotus, LjNBCL1 is involved in leaf patterning and participates in the regulation of axillary outgrowth. Wild-type Lotus leaves are composed of five leaflets and possess a pair of nectaries at the leaf axil. Legumes such as pea and Medicago have a pair of stipules, rather than nectaries, at the base of their leaves. In Ljnbcl1, nectary development is abolished, demonstrating that nectaries and stipules share a common evolutionary origin. In addition, ectopic roots arising from nodule vascular meristems and reorganization of the nodule vascular bundle vessels were observed on Ljnbcl1 nodules. This demonstrates that NBCL functions are conserved in both indeterminate and determinate nodules through the maintenance of nodule vascular bundle identity. In contrast to its role in floral patterning described in other plants, LjNBCL1 appears essential for the development of both secondary inflorescence meristem and floral meristem.This work was supported by the CNRS and by the grants ANR-14-CE19-0003 (NOOT) from the Agence National de la Recherche (ANR) to PR. This work has benefited from the facilities and expertise of the Servicio de Microscopia Electronica Universitat Politecnica de Valencia (Spain, http://www.upv.es/entidades/SME/) and of the IMAGIF Cell Biology Unit of the Gif campus (France, www.imagif.cnrs.fr) which is supported by the Conseil General de l'Essonne. The authors thank Dr Mathias Brault from the Institute of Plant Sciences Paris-Saclay (France) for providing the pFRN: RNAi plasmid, A. rhizogenes ARqua1 strain and control GUS:RNAi construction, and Dr Simona Radutoiu from the University of Aarhus (Denmark), for providing the Na-Borate/TRIZOL RNA extraction protocol. We are grateful to Dr Cristina Ferrandiz from the Instituto de Biologia Molecular y Celular de Plantas (Spain) for help in interpreting the identity of the meristems in the SEM pictures and Professor Frederique Guinel from the University of Wilfrid Laurier (Canada) for help in interpreting the identity of L. japonicus nodule vascular tissues. We thank Dr Julie Hofer from the University of Auckland (New Zealand), for manuscript revision and English language polishing.Magne, K.; George, J.; Berbel Tornero, A.; Broquet, B.; Madueño Albi, F.; Andersen, S.; Ratet, P. (2018). Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development. The Plant Journal. 94(5):880-894. https://doi.org/10.1111/tpj.13905S880894945Aida, M., & Tasaka, M. (2006). Genetic control of shoot organ boundaries. Current Opinion in Plant Biology, 9(1), 72-77. doi:10.1016/j.pbi.2005.11.011Aida, M., & Tasaka, M. (2006). Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex. Plant Molecular Biology, 60(6), 915-928. doi:10.1007/s11103-005-2760-7Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell, 9(6), 841-857. doi:10.1105/tpc.9.6.841AKASAKA, Y. (1998). Morphological Alterations and Root Nodule Formation inAgrobacterium rhizogenes-mediated Transgenic Hairy Roots of Peanut (Arachis hypogaeaL.). Annals of Botany, 81(2), 355-362. doi:10.1006/anbo.1997.0566Benlloch, R., Berbel, A., Ali, L., Gohari, G., Millán, T., & Madueño, F. (2015). Genetic control of inflorescence architecture in legumes. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.00543Berbel, A., Ferrándiz, C., Hecht, V., Dalmais, M., Lund, O. S., Sussmilch, F. C., … Madueño, F. (2012). VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nature Communications, 3(1). doi:10.1038/ncomms1801Blázquez, M. A., Ferrándiz, C., Madueño, F., & Parcy, F. (2006). How Floral Meristems are Built. Plant Molecular Biology, 60(6), 855-870. doi:10.1007/s11103-006-0013-zBrown, S. M., Oparka, K. J., Sprent, J. I., & Walsh, K. B. (1995). Symplastic transport in soybean root nodules. Soil Biology and Biochemistry, 27(4-5), 387-399. doi:10.1016/0038-0717(95)98609-rChen, Y., Chen, W., Li, X., Jiang, H., Wu, P., Xia, K., … Wu, G. (2013). Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant and Cell Physiology, 55(1), 183-193. doi:10.1093/pcp/pct171Cho, E., & Zambryski, P. C. (2011). ORGAN BOUNDARY1defines a gene expressed at the junction between the shoot apical meristem and lateral organs. Proceedings of the National Academy of Sciences, 108(5), 2154-2159. doi:10.1073/pnas.1018542108Couzigou, J.-M., & Ratet, P. (2015). NOOT-Dependent Control of Nodule Identity: Nodule Homeosis and Merirostem Perturbation. Biological Nitrogen Fixation, 487-498. doi:10.1002/9781119053095.ch49Couzigou, J.-M., Zhukov, V., Mondy, S., Abu el Heba, G., Cosson, V., Ellis, T. H. N., … Ratet, P. (2012). NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes. The Plant Cell, 24(11), 4498-4510. doi:10.1105/tpc.112.103747Couzigou, J.-M., Magne, K., Mondy, S., Cosson, V., Clements, J., & Ratet, P. (2015). The legume NOOT-BOP-COCH-LIKE genes are conserved regulators of abscission, a major agronomical trait in cultivated crops. New Phytologist, 209(1), 228-240. doi:10.1111/nph.13634Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., & Scheible, W.-R. (2005). Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis. Plant Physiology, 139(1), 5-17. doi:10.1104/pp.105.063743Dong, Z., Zhao, Z., Liu, C., Luo, J., Yang, J., Huang, W., … Luo, D. (2005). Floral Patterning in Lotus japonicus. Plant Physiology, 137(4), 1272-1282. doi:10.1104/pp.104.054288Ehrhardt, D., Atkinson, E., & Long. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science, 256(5059), 998-1000. doi:10.1126/science.10744524Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Cai, Z., … Luo, D. (2006). Control of petal shape and floral zygomorphy in Lotus japonicus. Proceedings of the National Academy of Sciences, 103(13), 4970-4975. doi:10.1073/pnas.0600681103Ferguson, B. J., & Reid, J. B. (2005). Cochleata: Getting to the Root of Legume Nodules. Plant and Cell Physiology, 46(9), 1583-1589. doi:10.1093/pcp/pci171Ferraioli, S., Tatè, R., Rogato, A., Chiurazzi, M., & Patriarca, E. J. (2004). Development of Ectopic Roots from Abortive Nodule Primordia. Molecular Plant-Microbe Interactions®, 17(10), 1043-1050. doi:10.1094/mpmi.2004.17.10.1043Franssen, H. J., Xiao, T. T., Kulikova, O., Wan, X., Bisseling, T., Scheres, B., & Heidstra, R. (2015). Root developmental programs shape the Medicago truncatula nodule meristem. Development, 142(17), 2941-2950. doi:10.1242/dev.120774Gonzalez-Rizzo, S., Crespi, M., & Frugier, F. (2006). The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti. The Plant Cell, 18(10), 2680-2693. doi:10.1105/tpc.106.043778Gourion, B., Sulser, S., Frunzke, J., Francez-Charlot, A., Stiefel, P., Pessi, G., … Fischer, H.-M. (2009). The PhyR-σEcfGsignalling cascade is involved in stress response and symbiotic efficiency inBradyrhizobium japonicum. Molecular Microbiology, 73(2), 291-305. doi:10.1111/j.1365-2958.2009.06769.xGourlay, C. W., Hofer, J. M. I., & Ellis, T. H. N. (2000). Pea Compound Leaf Architecture Is Regulated by Interactions among the Genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS. The Plant Cell, 12(8), 1279-1294. doi:10.1105/tpc.12.8.1279Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M. K., & Bonfante, P. (2009). Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist, 182(1), 200-212. doi:10.1111/j.1469-8137.2008.02725.xGuinel, F. C. (2009). Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types. Botany, 87(12), 1117-1138. doi:10.1139/b09-074Ha, C. M. (2003). The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development, 130(1), 161-172. doi:10.1242/dev.00196Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2004). BLADE-ON-PETIOLE1 Encodes a BTB/POZ Domain Protein Required for Leaf Morphogenesis in Arabidopsis thaliana. Plant and Cell Physiology, 45(10), 1361-1370. doi:10.1093/pcp/pch201Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2007). BLADE-ON-PETIOLE1 and 2 Control Arabidopsis Lateral Organ Fate through Regulation of LOB Domain and Adaxial-Abaxial Polarity Genes. The Plant Cell, 19(6), 1809-1825. doi:10.1105/tpc.107.051938Handberg, K., & Stougaard, J. (1992). Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal, 2(4), 487-496. doi:10.1111/j.1365-313x.1992.00487.xHepworth, S. R., & Pautot, V. A. (2015). Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01052Hepworth, S. R., Zhang, Y., McKim, S., Li, X., & Haughn, G. W. (2005). BLADE-ON-PETIOLE–Dependent Signaling Controls Leaf and Floral Patterning in Arabidopsis. The Plant Cell, 17(5), 1434-1448. doi:10.1105/tpc.104.030536Hepworth, S. R., Klenz, J. E., & Haughn, G. W. (2005). UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta, 223(4), 769-778. doi:10.1007/s00425-005-0138-3Hibara, K., Karim, M. R., Takada, S., Taoka, K., Furutani, M., Aida, M., & Tasaka, M. (2006). Arabidopsis CUP-SHAPED COTYLEDON3 Regulates Postembryonic Shoot Meristem and Organ Boundary Formation. The Plant Cell, 18(11), 2946-2957. doi:10.1105/tpc.106.045716Høgslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M. A., Goffard, N., … Stougaard, J. (2009). Dissection of Symbiosis and Organ Development by Integrated Transcriptome Analysis of Lotus japonicus Mutant and Wild-Type Plants. PLoS ONE, 4(8), e6556. doi:10.1371/journal.pone.0006556JARVIS, B. D. W., PANKHURST, C. E., & PATEL, J. J. (1982). Rhizobium loti, a New Species of Legume Root Nodule Bacteria. International Journal of Systematic Bacteriology, 32(3), 378-380. doi:10.1099/00207713-32-3-378Karim, M. R., Hirota, A., Kwiatkowska, D., Tasaka, M., & Aida, M. (2009). A Role for Arabidopsis PUCHI in Floral Meristem Identity and Bract Suppression. The Plant Cell, 21(5), 1360-1372. doi:10.1105/tpc.109.067025Khan, M., Xu, M., Murmu, J., Tabb, P., Liu, Y., Storey, K., … Hepworth, S. R. (2011). Antagonistic Interaction of BLADE-ON-PETIOLE1 and 2 with BREVIPEDICELLUS and PENNYWISE Regulates Arabidopsis Inflorescence Architecture. Plant Physiology, 158(2), 946-960. doi:10.1104/pp.111.188573Koch, B., & Evans, H. J. (1966). Reduction of Acetylene to Ethylene by Soybean Root Nodules. Plant Physiology, 41(10), 1748-1750. doi:10.1104/pp.41.10.1748Krall, L., Wiedemann, U., Unsin, G., Weiss, S., Domke, N., & Baron, C. (2002). Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, 99(17), 11405-11410. doi:10.1073/pnas.172390699Kumagai, H., & Kouchi, H. (2003). Gene Silencing by Expression of Hairpin RNA in Lotus japonicus Roots and Root Nodules. Molecular Plant-Microbe Interactions®, 16(8), 663-668. doi:10.1094/mpmi.2003.16.8.663Levin, J. Z., & Meyerowitz, E. M. (1995). UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. The Plant Cell, 7(5), 529-548. doi:10.1105/tpc.7.5.529Long, J., & Barton, M. K. (2000). Initiation of Axillary and Floral Meristems in Arabidopsis. Developmental Biology, 218(2), 341-353. doi:10.1006/dbio.1999.9572Małolepszy, A., Mun, T., Sandal, N., Gupta, V., Dubin, M., Urbański, D., … Andersen, S. U. (2016). The LORE 1 insertion mutant resource. The Plant Journal, 88(2), 306-317. doi:10.1111/tpj.13243McKim, S. M., Stenvik, G.-E., Butenko, M. A., Kristiansen, W., Cho, S. K., Hepworth, S. R., … Haughn, G. W. (2008). The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development, 135(8), 1537-1546. doi:10.1242/dev.012807Mun, T., Bachmann, A., Gupta, V., Stougaard, J., & Andersen, S. U. (2016). Lotus Base: An integrated information portal for the model legume Lotus japonicus. Scientific Reports, 6(1). doi:10.1038/srep39447Norberg, M. (2005). The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development, 132(9), 2203-2213. doi:10.1242/dev.01815Okamoto, S., Yoro, E., Suzaki, T., & Kawaguchi, M. (2013). Hairy Root Transformation in Lotus japonicus. BIO-PROTOCOL, 3(12). doi:10.21769/bioprotoc.795Oldroyd, G. E. D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology, 11(4), 252-263. doi:10.1038/nrmicro2990Oldroyd, G. E. D., & Downie, J. A. (2008). Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes. Annual Review of Plant Biology, 59(1), 519-546. doi:10.1146/annurev.arplant.59.032607.092839Pate, J. S., Gunning, B. E. S., & Briarty, L. G. (1969). Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta, 85(1), 11-34. doi:10.1007/bf00387658Ping, J., Liu, Y., Sun, L., Zhao, M., Li, Y., She, M., … Ma, J. (2014). Dt2 Is a Gain-of-Function MADS-Domain Factor Gene That Specifies Semideterminacy in Soybean. The Plant Cell, 26(7), 2831-2842. doi:10.1105/tpc.114.126938Quandt, H.-J. (1993). Transgenic Root Nodules ofVicia hirsuta:A Fast and Efficient System for the Study of Gene Expression in Indeterminate-Type Nodules. Molecular Plant-Microbe Interactions, 6(6), 699. doi:10.1094/mpmi-6-699Roux, B., Rodde, N., Jardinaud, M.-F., Timmers, T., Sauviac, L., Cottret, L., … Gamas, P. (2014). An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. The Plant Journal, 77(6), 817-837. doi:10.1111/tpj.12442Schultz, E. A., & Haughn, G. W. (1991). LEAFY, a Homeotic Gene That Regulates Inflorescence Development in Arabidopsis. The Plant Cell, 771-781. doi:10.1105/tpc.3.8.771Sinharoy, S., & DasGupta, M. (2009). RNA Interference Highlights the Role of CCaMK in Dissemination of Endosymbionts in the Aeschynomeneae Legume Arachis. Molecular Plant-Microbe Interactions®, 22(11), 1466-1475. doi:10.1094/mpmi-22-11-1466Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., & Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, 92(7), 2647-2651. doi:10.1073/pnas.92.7.2647Soyano, T., Kouchi, H., Hirota, A., & Hayashi, M. (2013). NODULE INCEPTION Directly Targets NF-Y Subunit Genes to Regulate Essential Processes of Root Nodule Development in Lotus japonicus. PLoS Genetics, 9(3), e1003352. doi:10.1371/journal.pgen.1003352Suzaki, T., Yoro, E., & Kawaguchi, M. (2015). Leguminous Plants: Inventors of Root Nodules to Accommodate Symbiotic Bacteria. International Review of Cell and Molecular Biology, 111-158. doi:10.1016/bs.ircmb.2015.01.004Takeda, S., Hanano, K., Kariya, A., Shimizu, S., Zhao, L., Matsui, M., … Aida, M. (2011). CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. The Plant Journal, 66(6), 1066-1077. doi:10.1111/j.1365-313x.2011.04571.xTavakol, E., Okagaki, R., Verderio, G., Shariati J., V., Hussien, A., Bilgic, H., … Rossini, L. (2015). The Barley Uniculme4 Gene Encodes a BLADE-ON-PETIOLE-Like Protein That Controls Tillering and Leaf Patterning. Plant Physiology, 168(1), 164-174. doi:10.1104/pp.114.252882Udvardi, M., & Poole, P. S. (2013). Transport and Metabolism in Legume-Rhizobia Symbioses. Annual Review of Plant Biology, 64(1), 781-805. doi:10.1146/annurev-arplant-050312-120235Van de Velde, W., Guerra, J. C. P., Keyser, A. D., De Rycke, R., Rombauts, S., Maunoury, N., … Goormachtig, S. (2006). Aging in Legume Symbiosis. A Molecular View on Nodule Senescence in Medicago truncatula. Plant Physiology, 141(2), 711-720. doi:10.1104/pp.106.078691Verdier, J., Torres-Jerez, I., Wang, M., Andriankaja, A., Allen, S. N., He, J., … Udvardi, M. K. (2013). Establishment of theLotus japonicusGene Expression Atlas (LjGEA) and its use to explore legume seed maturation. The Plant Journal, 74(2), 351-362. doi:10.1111/tpj.12119WALSH, K. B., McCULLY, M. E., & CANNY, M. J. (1989). Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway. Plant, Cell and Environment, 12(4), 395-405. doi:10.1111/j.1365-3040.1989.tb01955.xWang, Q., Hasson, A., Rossmann, S., & Theres, K. (2015). Divide et impera : boundaries shape the plant body and initiate new meristems. New Phytologist, 209(2), 485-498. doi:10.1111/nph.13641Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., … Yang, J. (2011). Petal Development in Lotus japonicus. Journal of Integrative Plant Biology, 53(10), 770-782. doi:10.1111/j.1744-7909.2011.01072.xWerner, G. D. A., Cornwell, W. K., Sprent, J. I., Kattge, J., & Kiers, E. T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Communications, 5(1). doi:10.1038/ncomms5087Wopereis, J., Pajuelo, E., Dazzo, F. B., Jiang, Q., Gresshoff, P. M., de Bruijn, F. J., … Szczyglowski, K. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal, 23(1), 97-114. doi:10.1046/j.1365-313x.2000.00799.xWu, X.-M., Yu, Y., Han, L.-B., Li, C.-L., Wang, H.-Y., Zhong, N.-Q., … Xia, G.-X. (2012). The Tobacco BLADE-ON-PETIOLE2 Gene Mediates Differentiation of the Corolla Abscission Zone by Controlling Longitudinal Cell Expansion. Plant Physiology, 159(2), 835-850. doi:10.1104/pp.112.193482Xu, M., Hu, T., McKim, S. M., Murmu, J., Haughn, G. W., & Hepworth, S. R. (2010). Arabidopsis BLADE-ON-PETIOLE1 and 2 promote floral meristem fate and determinacy in a previously undefined pathway targeting APETALA1 and AGAMOUS-LIKE24. The Plant Journal, 63(6), 974-989. doi:10.1111/j.1365-313x.2010.04299.xXu, C., Park, S. J., Van Eck, J., & Lippman, Z. B. (2016). Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes & Development, 30(18), 2048-2061. doi:10.1101/gad.288415.116Yaxley, J. (2001). Leaf and Flower Development in Pea (Pisum sativum L.): Mutants cochleata andunifoliata. Annals of Botany, 88(2), 225-234. doi:10.1006/anbo.2001.1448Žádníková, P., & Simon, R. (2014). How boundaries control plant development. Current Opinion in Plant Biology, 17, 116-125. doi:10.1016/j.pbi.2013.11.013Zhang, S., Sandal, N., Polowick, P. L., Stiller, J., Stougaard, J., & Fobert, P. R. (2003). Proliferating Floral Organs (Pfo ), a Lotus japonicus gene required for specifying floral meristem determinacy and organ identity, encodes an F-box protein. The Plant Journal, 33(4), 607-619. doi:10.1046/j.1365-313x.2003.01660.

Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration

Author Posting. © American Geophysical Union, 2012. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research 117 (2012): G03002, doi:10.1029/2012JG001949.Until recently, the process of denitrification (conversion of nitrate or nitrite to gaseous products) was thought to be performed exclusively by prokaryotes and fungi. The finding that foraminifera perform complete denitrification could impact our understanding of nitrate removal in sediments as well as our understanding of eukaryotic respiration, especially if it is widespread. However, details of this process and the subcellular location of these reactions in foraminifera remain uncertain. For example, prokaryotic endobionts, rather than the foraminifer proper, could perform denitrification, as has been shown recently in an allogromiid foraminifer. Here, intracellular nitrate concentrations and isotope ratios (δ15NNO3 and δ18ONO3) were measured to assess the nitrate dynamics in four benthic foraminiferal species (Bolivina argentea, Buliminella tenuata, Fursenkoina cornuta, Nonionella stella) with differing cellular architecture and associations with microbial endobionts, recovered from Santa Barbara Basin, California. Cellular nitrate concentrations were high (12–217 mM) in each species, and intracellular nitrate often had elevated δ15NNO3 and δ18ONO3 values. Experiments including suboxic and anoxic incubations of B. argentea revealed a decrease in intracellular nitrate concentration and an increase in δ15NNO3 and δ18ONO3 over time, indicating nitrate respiration and/or denitrification within the foraminifera. Results illustrate that nitrate reduction occurs in a range of foraminiferal species, including some possessing endobionts (including a chloroplast-sequestering species) and others lacking endobionts, implying that microbial associates may not solely be responsible for this process in foraminifera. Furthermore, we show that benthic foraminifera may represent important reservoirs of nitrate storage in sediments, as well as mediators of its removal.This research was supported by NSF grant EF-0702491 to JMB, KLC, and VPE.2013-01-0

Denitrification likely catalyzed by endobionts in an allogromiid foraminifer

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of Nature Publishing Group for personal use, not for redistribution. The definitive version was published in The ISME Journal 6 (2012): 951–960, doi:10.1038/ismej.2011.171.Nitrogen can be a limiting macronutrient for carbon uptake by the marine biosphere. The process of denitrification (conversion of nitrate to gaseous compounds, including N2) removes bioavailable nitrogen, particularly in marine sediments, making it a key factor in the marine nitrogen budget. Benthic foraminifera reportedly perform complete denitrification, a process previously considered nearly exclusively performed by bacteria and archaea. If the ability to denitrify is widespread among these diverse and abundant protists, a paradigm shift is required for biogeochemistry and marine microbial ecology. However, to date, the mechanisms of foraminiferal denitrification are unclear and it is possible that the ability to perform complete denitrification is due to symbiont metabolism in some foraminiferal species. Using sequence analysis and GeneFISH, we show that for a symbiont-bearing foraminifer, the potential for denitrification resides in the endobionts. Results also identify the endobionts as denitrifying pseudomonads and show that the allogromiid accumulates nitrate intracellularly, presumably for use in denitrification. Endobionts have been observed within many foraminiferal species, and in the case of associations with denitrifying bacteria, may provide fitness for survival in anoxic conditions. These associations may have been a driving force for early foraminiferal diversification, which is thought to have occurred in the Neoproterozoic when anoxia was widespread.This research was supported by NSF grant EF-0702491 to JMB, KLC and VPE; some ship support was provided by NSF MCB-0604084 to VPE and JMB.2012-06-0

Genetic diversity and connectivity within Mytilus spp. in the subarctic and Arctic

Climate changes in the Arctic are predicted to alter distributions of marine species. However, such changes are difficult to quantify because information on present species distribution and the genetic variation within species is lacking or poorly examined. Blue mussels,Mytilusspp. are ecosystem engineers in the coastal zone globally. In order to improve knowledge of distribution and genetic structure of theMytilus eduliscomplex in the Arctic, we analyzed 81 SNPs in 534Mytilusspp. individuals sampled at 13 sites to provide baseline data for distribution and genetic variation ofMytilusmussels in the European Arctic.Mytilus eduliswas the most abundant species found with a clear genetic split between populations in Greenland and the Eastern Atlantic. Surprisingly, analyses revealed the presence ofM. trossulusin high Arctic NW Greenland (77°N) andM. galloprovincialisor their hybrids in SW Greenland, Svalbard and the Pechora Sea. Furthermore, a high degree of hybridization and introgression between species was observed. Our study highlights the importance of distinguishing between congener species, which can display local adaptation and suggests that information on dispersal routes and barriers are essential for accurate predictions of regional susceptibility to range expansions or invasions of boreal species in the Arctic

Comparative Functional Genomics of Salt Stress in Related Model and Cultivated Plants Identifies and Overcomes Limitations to Translational Genomics

One of the objectives of plant translational genomics is to use knowledge and genes discovered in model species to improve crops. However, the value of translational genomics to plant breeding, especially for complex traits like abiotic stress tolerance, remains uncertain. Using comparative genomics (ionomics, transcriptomics and metabolomics) we analyzed the responses to salinity of three model and three cultivated species of the legume genus Lotus. At physiological and ionomic levels, models responded to salinity in a similar way to crop species, and changes in the concentration of shoot Cl− correlated well with tolerance. Metabolic changes were partially conserved, but divergence was observed amongst the genotypes. Transcriptome analysis showed that about 60% of expressed genes were responsive to salt treatment in one or more species, but less than 1% was responsive in all. Therefore, genotype-specific transcriptional and metabolic changes overshadowed conserved responses to salinity and represent an impediment to simple translational genomics. However, ‘triangulation’ from multiple genotypes enabled the identification of conserved and tolerant-specific responses that may provide durable tolerance across species