Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)

Bird, Toby; Nestor, Benjamin J.; Bayer, Philipp E.; Wang, Guannan; Ilyasova, Albina; Gille, Clément E.; Soraru, Bryce E. H.; Ranathunge, Kosala; Severn-Ellis, Anita A.; Jost, Ricarda; Scheible, Wolf-Rüdiger; Dassanayake, Maheshi; Batley, Jacqueline; Edwards, David; Lambers, Hans; Finnegan, Patrick M.

doi:10.1007/s11104-023-06275-1

Title: Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)

Journal Article · 27 September 2023 · Plant and Soil

DOI: https://doi.org/10.1007/s11104-023-06275-1 · OSTI ID:2006682

;

; Ilyasova, Albina;

; Soraru, Bryce E. H.;

;

Abstract Background and aims Hakea prostrata (Proteaceae) is a highly phosphorus-use-efficient plant native to southwest Australia. It maintains a high photosynthetic rate at low leaf phosphorus (P) and exhibits delayed leaf greening, a convergent adaptation that increases nutrient-use efficiency. This study aimed to provide broad physiological and gene expression profiles across leaf development, uncovering pathways leading from young leaves as nutrient sinks to mature leaves as low-nutrient, energy-transducing sources. Methods To explore gene expression underlying delayed greening, we analysed a de novo transcriptome for H. prostrata across five stages of leaf development. Photosynthesis and respiration rates, and foliar pigment, P and nitrogen (N) concentrations were determined, including the division of P into five biochemical fractions. Key results Transcripts encoding functions associated with leaf structure generally decreased in abundance across leaf development, concomitant with decreases in foliar concentrations of 85% for anthocyanins, 90% for P and 70% for N. The expression of genes associated with photosynthetic function increased during or after leaf expansion, in parallel with increases in photosynthetic pigments and activity, much later in leaf development than in species that do not have delayed greening. As leaves developed, transcript abundance for cytosolic and mitochondrial ribosomal proteins generally declined, whilst transcripts for chloroplast ribosomal proteins increased. Conclusions There was a much longer temporal separation of leaf cell growth from chloroplast development in H. prostrata than is found in species that lack delayed greening. Transcriptome-guided analysis of leaf development in H. prostrata provided insight into delayed greening as a nutrient-saving strategy in severely phosphorus-impoverished landscapes.

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Sponsoring Organization:: USDOE

OSTI ID:: 2006682

Journal Information:: Plant and Soil, Journal Name: Plant and Soil Journal Issue: 1-2 Vol. 496; ISSN 0032-079X

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (75)

Characterization and Measurement of Anthocyanins by UV‐Visible Spectroscopy Giusti, M. Mónica; Wrolstad, Ronald E. Current Protocols in Food Analytical Chemistry, Vol. 00, Issue 1 https://doi.org/10.1002/0471142913.faf0102s00	journal	April 2001
Cell Cycling and Cell Enlargement in Developing Leaves of Arabidopsis Donnelly, Petra M.; Bonetta, Dario; Tsukaya, Hirokazu Developmental Biology, Vol. 215, Issue 2 https://doi.org/10.1006/dbio.1999.9443	journal	November 1999
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Data Analysis Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4_9	book	June 2016
Soil Development and Nutrient Availability Along a 2 Million-Year Coastal Dune Chronosequence Under Species-Rich Mediterranean Shrubland in Southwestern Australia Turner, Benjamin L.; Laliberté, Etienne Ecosystems, Vol. 18, Issue 2 https://doi.org/10.1007/s10021-014-9830-0	journal	December 2014
Cluster Roots: A Curiosity in Context Shane, Michael W.; Lambers, Hans Plant and Soil, Vol. 274, Issue 1-2 https://doi.org/10.1007/s11104-004-2725-7	journal	July 2005
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
The Spectral Determination of Chlorophylls a and b, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution Wellburn, Alan R. Journal of Plant Physiology, Vol. 144, Issue 3 https://doi.org/10.1016/S0176-1617(11)81192-2	journal	September 1994
Exit from Proliferation during Leaf Development in Arabidopsis thaliana: A Not-So-Gradual Process Andriankaja, Megan; Dhondt, Stijn; De Bodt, Stefanie Developmental Cell, Vol. 22, Issue 1 https://doi.org/10.1016/j.devcel.2011.11.011	journal	January 2012
Determination of major and trace elements in biological materials by microwave induced plasma optical emission spectrometry (MIP-OES) following tetramethylammonium hydroxide (TMAH) solubilization Matusiewicz, Henryk; Golik, Bartosz Microchemical Journal, Vol. 76, Issue 1-2 https://doi.org/10.1016/j.microc.2003.10.007	journal	February 2004
Leaf growth in dicots and monocots: so different yet so alike Nelissen, Hilde; Gonzalez, Nathalie; Inzé, Dirk Current Opinion in Plant Biology, Vol. 33 https://doi.org/10.1016/j.pbi.2016.06.009	journal	October 2016
Ribosomal composition and control of leaf development Schippers, Jos H. M.; Mueller-Roeber, Bernd Plant Science, Vol. 179, Issue 4 https://doi.org/10.1016/j.plantsci.2010.06.012	journal	October 2010
Unveiling the functions of plastid ribosomal proteins in plant development and abiotic stress tolerance Robles, Pedro; Quesada, Víctor Plant Physiology and Biochemistry, Vol. 189 https://doi.org/10.1016/j.plaphy.2022.07.029	journal	October 2022
Tracking color and pigment changes in anthocyanin products Wrolstad, Ronald E.; Durst, Robert W.; Lee, Jungmin Trends in Food Science & Technology, Vol. 16, Issue 9 https://doi.org/10.1016/j.tifs.2005.03.019	journal	September 2005
clusterProfiler 4.0: A universal enrichment tool for interpreting omics data Wu, Tianzhi; Hu, Erqiang; Xu, Shuangbin The Innovation, Vol. 2, Issue 3 https://doi.org/10.1016/j.xinn.2021.100141	journal	August 2021
De novo full length transcriptome analysis of Arachis glabrata provides insights into gene expression dynamics in response to biotic and abiotic stresses Zhao, Chuanzhi; He, Liangqiong; Xia, Han Genomics, Vol. 113, Issue 3 https://doi.org/10.1016/j.ygeno.2021.03.030	journal	May 2021
Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. Shane, Michael W.; de Vos, Martin; de Roock, Sytze Plant and Soil, Vol. 248, Issue 1/2 https://doi.org/10.1023/A:1022320416038	journal	January 2003
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
The worldwide leaf economics spectrum Wright, Ian J.; Reich, Peter B.; Westoby, Mark Nature, Vol. 428, Issue 6985 https://doi.org/10.1038/nature02403	journal	April 2004
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice Wang, Lin; Czedik-Eysenberg, Angelika; Mertz, Rachel A. Nature Biotechnology, Vol. 32, Issue 11 https://doi.org/10.1038/nbt.3019	journal	October 2014
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
The developmental dynamics of the maize leaf transcriptome Li, Pinghua; Ponnala, Lalit; Gandotra, Neeru Nature Genetics, Vol. 42, Issue 12, p. 1060-1067 https://doi.org/10.1038/ng.703	journal	October 2010
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran Nature Protocols, Vol. 8, Issue 8 https://doi.org/10.1038/nprot.2013.084	journal	July 2013
Chromosome-level assemblies of multiple Arabidopsis genomes reveal hotspots of rearrangements with altered evolutionary dynamics Jiao, Wen-Biao; Schneeberger, Korbinian Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14779-y	journal	February 2020
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
Sensitive protein alignments at tree-of-life scale using DIAMOND Buchfink, Benjamin; Reuter, Klaus; Drost, Hajk-Georg Nature Methods, Vol. 18, Issue 4 https://doi.org/10.1038/s41592-021-01101-x	journal	April 2021
Changes in mesophyll anatomy and sink-source relationships during leaf development in Quercus glauca , an evergreen tree showing delayed leaf greening Miyazawa, S. -I.; Makino, A.; Terashima, I. Plant, Cell & Environment, Vol. 26, Issue 5 https://doi.org/10.1046/j.1365-3040.2003.01011.x	journal	May 2003
Delayed greening in phosphorus-efficient Hakea prostrata (Proteaceae) is a photoprotective and nutrient-saving strategy Kuppusamy, Thirumurugen; Hahne, Dorothee; Ranathunge, Kosala Functional Plant Biology, Vol. 48, Issue 2 https://doi.org/10.1071/FP19285	journal	January 2021
From tropics to tundra: Global convergence in plant functioning Reich, P. B.; Walters, M. B.; Ellsworth, D. S. Proceedings of the National Academy of Sciences, Vol. 94, Issue 25 https://doi.org/10.1073/pnas.94.25.13730	journal	December 1997
Food colorants: Anthocyanins Francis, F. J.; Markakis, Pericles C. Critical Reviews in Food Science and Nutrition, Vol. 28, Issue 4 https://doi.org/10.1080/10408398909527503	journal	January 1989
BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks Maere, S.; Heymans, K.; Kuiper, M. Bioinformatics, Vol. 21, Issue 16 https://doi.org/10.1093/bioinformatics/bti551	journal	June 2005
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
A De Novo Transcriptome Assembly ofCeratopteris richardiiProvides Insights into the Evolutionary Dynamics of Complex Gene Families in Land Plants Geng, Yuan; Cai, Chao; McAdam, Scott A. M. Genome Biology and Evolution, Vol. 13, Issue 3 https://doi.org/10.1093/gbe/evab042	journal	March 2021
Do anthocyanins play a role in UV protection of the red juvenile leaves of Syzygium? Woodall, G. S.; Stewart, G. R. Journal of Experimental Botany, Vol. 49, Issue 325 https://doi.org/10.1093/jxb/49.325.1447	journal	August 1998
BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes Manni, Mosè; Berkeley, Matthew R.; Seppey, Mathieu Molecular Biology and Evolution, Vol. 38, Issue 10 https://doi.org/10.1093/molbev/msab199	journal	July 2021
The Gene Ontology resource: enriching a GOld mine Carbon, Seth; Douglass, Eric; Good, Benjamin M. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1113	journal	December 2020
Database resources of the National Center for Biotechnology Information Wheeler, D. L.; Barrett, T.; Benson, D. A. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl1031	journal	January 2007
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
UniProt: a hub for protein information Consortium, UniPot Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212 https://doi.org/10.1093/nar/gku989	journal	October 2014
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Huerta-Cepas, Jaime; Szklarczyk, Damian; Heller, Davide Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1085	journal	November 2018
The Pfam protein families database in 2019 El-Gebali, Sara; Mistry, Jaina; Bateman, Alex Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky995	journal	October 2018
Photorespiration: metabolic pathways and their role in stress protection Wingler, Astrid; Lea, Peter J.; Quick, W. Paul Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0712	journal	October 2000
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Genome-Wide Analysis of Gene Expression Profiles Associated with Cell Cycle Transitions in Growing Organs of Arabidopsis Beemster, Gerrit T. S.; De Veylder, Lieven; Vercruysse, Steven Plant Physiology, Vol. 138, Issue 2 https://doi.org/10.1104/pp.104.053884	journal	April 2005
Lipid Biosynthesis and Protein Concentration Respond Uniquely to Phosphate Supply during Leaf Development in Highly Phosphorus-Efficient Hakea prostrata Kuppusamy, Thirumurugen; Giavalisco, Patrick; Arvidsson, Samuel Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.248930	journal	October 2014
Delayed greening during leaf expansion under ambient and elevated CO₂ in tropical tree seedlings Vogado, Nara O.; Cheesman, Alexander W.; Cernusak, Lucas A. Austral Ecology, Vol. 47, Issue 3 https://doi.org/10.1111/aec.13139	journal	December 2021
The consequences of delayed greening during leaf development for light absorption and light use efficiency Kursar, T. A.; Coley, P. D. Plant, Cell and Environment, Vol. 15, Issue 8 https://doi.org/10.1111/j.1365-3040.1992.tb01022.x	journal	October 1992
Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species Hughes, Nicole M.; Morley, Christianna B.; Smith, William K. New Phytologist, Vol. 175, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02133.x	journal	September 2007
Opportunities for improving phosphorus-use efficiency in crop plants: Tansley review Veneklaas, Erik J.; Lambers, Hans; Bragg, Jason New Phytologist, Vol. 195, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04190.x	journal	June 2012
Proteaceae from severely phosphorus‐impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus‐use‐efficiency Lambers, Hans; Cawthray, Gregory R.; Giavalisco, Patrick New Phytologist, Vol. 196, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04285.x	journal	August 2012
Responses of foliar phosphorus fractions to soil age are diverse along a 2 Myr dune chronosequence Yan, Li; Zhang, Xinhou; Han, Zhongming New Phytologist, Vol. 223, Issue 3 https://doi.org/10.1111/nph.15910	journal	June 2019
Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus‐use efficiency of P roteaceae species Sulpice, Ronan; Ishihara, Hirofumi; Schlereth, Armin Plant, Cell & Environment, Vol. 37, Issue 6 https://doi.org/10.1111/pce.12240	journal	December 2013
Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: An adaptation improving phosphorus-use efficiency: Allocation of phosphorus to photosynthetic cells Hayes, Patrick E.; Clode, Peta L.; Oliveira, Rafael S. Plant, Cell & Environment, Vol. 41, Issue 3 https://doi.org/10.1111/pce.13124	journal	January 2018
Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development: Different functions of plastid ribosome subunits Romani, Isidora; Tadini, Luca; Rossi, Fabio The Plant Journal, Vol. 72, Issue 6 https://doi.org/10.1111/tpj.12000	journal	October 2012
Phosphorus Acquisition and Utilization in Plants Lambers, Hans Annual Review of Plant Biology, Vol. 73, Issue 1 https://doi.org/10.1146/annurev-arplant-102720-125738	journal	May 2022
The Southwest Australian Floristic Region: Evolution and Conservation of a Global Hot Spot of Biodiversity Hopper, Stephen D.; Gioia, Paul Annual Review of Ecology, Evolution, and Systematics, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.ecolsys.35.112202.130201	journal	December 2004
Blast2GO: A Comprehensive Suite for Functional Analysis in Plant Genomics Conesa, Ana; Götz, Stefan International Journal of Plant Genomics, Vol. 2008 https://doi.org/10.1155/2008/619832	journal	January 2008
GOMCL: a toolkit to cluster, evaluate, and extract non-redundant associations of Gene Ontology-based functions Wang, Guannan; Oh, Dong-Ha; Dassanayake, Maheshi BMC Bioinformatics, Vol. 21, Issue 1 https://doi.org/10.1186/s12859-020-3447-4	journal	April 2020
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Cellular and transcriptomic analyses reveal two-staged chloroplast biogenesis underpinning photosynthesis build-up in the wheat leaf Loudya, Naresh; Mishra, Priyanka; Takahagi, Kotaro Genome Biology, Vol. 22, Issue 1 https://doi.org/10.1186/s13059-021-02366-3	journal	May 2021
Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads Song, Li; Florea, Liliana GigaScience, Vol. 4, Issue 1 https://doi.org/10.1186/s13742-015-0089-y	journal	October 2015
Leaf development and morphogenesis Bar, M.; Ori, N. Development, Vol. 141, Issue 22 https://doi.org/10.1242/dev.106195	journal	November 2014
Actin-mediated movement of chloroplasts Wada, Masamitsu; Kong, Sam-Geun Journal of Cell Science, Vol. 131, Issue 2 https://doi.org/10.1242/jcs.210310	journal	January 2018
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
The Ecophysiology of Foliar Anthocyanin Close, Dugald C.; Beadle, Christopher L. The Botanical Review, Vol. 69, Issue 2 https://doi.org/10.1663/0006-8101(2003)069[0149:TEOFA]2.0.CO;2	journal	April 2003
Delayed Greening in Tropical Leaves: An Antiherbivore Defense? Kursar, Thomas A.; Coley, Phyllis D. Biotropica, Vol. 24, Issue 2 https://doi.org/10.2307/2388520	journal	June 1992
Delayed Development of the Photosynthetic Apparatus in Tropical Rain Forest Species Kursar, T. A.; Coley, P. D. Functional Ecology, Vol. 6, Issue 4 https://doi.org/10.2307/2389279	journal	January 1992
Detecting sequence signals in targeting peptides using deep learning Almagro Armenteros, Jose Juan; Salvatore, Marco; Emanuelsson, Olof Life Science Alliance, Vol. 2, Issue 5 https://doi.org/10.26508/lsa.201900429	journal	September 2019
Leaf development: a cellular perspective Kalve, Shweta; De Vos, Dirk; Beemster, Gerrit T. S. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00362	journal	July 2014
Unraveling the Developmental and Genetic Mechanisms Underpinning Floral Architecture in Proteaceae Damerval, Catherine; Citerne, Hélène; Conde e. Silva, Natalia Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00018	journal	January 2019
Emerging Roles of Mitochondrial Ribosomal Proteins in Plant Development Robles, Pedro; Quesada, Víctor International Journal of Molecular Sciences, Vol. 18, Issue 12 https://doi.org/10.3390/ijms18122595	journal	December 2017
A multifaceted analysis reveals two distinct phases of chloroplast biogenesis during de-etiolation in Arabidopsis Pipitone, Rosa; Eicke, Simona; Pfister, Barbara eLife, Vol. 10 https://doi.org/10.7554/eLife.62709	journal	February 2021

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Title: Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)

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