A chloroplast localized heavy metal-associated domain containing protein regulates grain calcium accumulation in rice.
Oryza
/ metabolism
Chloroplasts
/ metabolism
Calcium
/ metabolism
Plant Proteins
/ metabolism
Animals
Gene Expression Regulation, Plant
Quantitative Trait Loci
Xenopus laevis
Oocytes
/ metabolism
Plant Leaves
/ metabolism
Metals, Heavy
/ metabolism
Plants, Genetically Modified
Edible Grain
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 Oct 2024
27 Oct 2024
Historique:
received:
01
12
2023
accepted:
16
10
2024
medline:
27
10
2024
pubmed:
27
10
2024
entrez:
27
10
2024
Statut:
epublish
Résumé
Calcium (Ca) is an essential mineral nutrient and plays a crucial signaling role in all living organisms. Increasing Ca content in staple foods such as rice is vital for improving Ca nutrition of humans. Here we map a quantitative trait locus that controls Ca concentration in rice grains and identify the causal gene as GCSC1 (Grain Ca and Sr Concentrations 1), which encodes a chloroplast vesicle localized homo-oligomeric protein. GCSC1 exhibits Ca
Identifiants
pubmed: 39462135
doi: 10.1038/s41467-024-53648-w
pii: 10.1038/s41467-024-53648-w
doi:
Substances chimiques
Calcium
SY7Q814VUP
Plant Proteins
0
Metals, Heavy
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9265Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31772382
Informations de copyright
© 2024. The Author(s).
Références
Cormick, G. & Belizan, J. M. Calcium intake and health. Nutrients 11, 1606 (2019).
pubmed: 31311164
pmcid: 6683260
doi: 10.3390/nu11071606
White, P. J. & Broadley, M. R. Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 182, 49–84 (2009).
pubmed: 19192191
doi: 10.1111/j.1469-8137.2008.02738.x
Kumssa, D. B. et al. Dietary calcium and zinc deficiency risks are decreasing but remain prevalent. Sci. Rep. 5, 10974 (2015).
pubmed: 26098577
pmcid: 4476434
doi: 10.1038/srep10974
Hirschi, K. D. Nutrient biofortification of food crops. Annu. Rev. Nutr. 29, 401–421 (2009).
pubmed: 19400753
doi: 10.1146/annurev-nutr-080508-141143
Jeong, J. & Guerinot, M. L. Biofortified and bioavailable: the gold standard, for plant-based diets. Proc. Natl. Acad. Sci. USA 105, 1777–1778 (2008).
pubmed: 18256182
pmcid: 2538837
doi: 10.1073/pnas.0712330105
McLaughlin, S. B. & Wimmer, R. Tansley review no. 104—Calcium physiology and terrestrial ecosystem processes. New Phytol. 142, 373–417 (1999).
doi: 10.1046/j.1469-8137.1999.00420.x
Luan, S. & Wang, C. Calcium signaling mechanisms across kingdoms. Annu. Rev. Cell. Dev. Biol. 37, 311–340 (2021).
pubmed: 34375534
doi: 10.1146/annurev-cellbio-120219-035210
McAinsh, M. R. & Pittman, J. K. Shaping the calcium signature. New Phytol. 181, 275–294 (2009).
pubmed: 19121028
doi: 10.1111/j.1469-8137.2008.02682.x
Kim, T. H., Bohmer, M., Hu, H., Nishimura, N. & Schroeder, J. I. Guard cell signal transduction network: advances in understanding abscisic acid, CO
pubmed: 20192751
pmcid: 3056615
doi: 10.1146/annurev-arplant-042809-112226
Demidchik, V., Shabala, S., Isayenkov, S., Cuin, T. A. & Pottosin, I. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220, 49–69 (2018).
pubmed: 29916203
doi: 10.1111/nph.15266
Teardo, E. et al. A chloroplast-localized mitochondrial calcium uniporter transduces osmotic stress in Arabidopsis. Nat. Plants 5, 581–588 (2019).
pubmed: 31182842
doi: 10.1038/s41477-019-0434-8
Frank, J. et al. Chloroplast-localized BICAT proteins shape stromal calcium signals and are required for efficient photosynthesis. New Phytol. 221, 866–880 (2019).
pubmed: 30169890
doi: 10.1111/nph.15407
Zhang, M. et al. Mapping and validation of quantitative trait loci associated with concentrations of 16 elements in unmilled rice grain. Theor. Appl. Genet. 127, 137–165 (2014).
pubmed: 24231918
doi: 10.1007/s00122-013-2207-5
Liu, H. et al. Univariate and multivariate QTL analyses reveal covariance among mineral elements in the rice ionome. Front. Genet. 12, 638555 (2021).
pubmed: 33569081
pmcid: 7868434
doi: 10.3389/fgene.2021.638555
Huang, X. Y. et al. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat. Commun 7, 12138 (2016).
pubmed: 27387148
pmcid: 4941113
doi: 10.1038/ncomms12138
Lindquist, E. & Aronsson, H. Chloroplast vesicle transport. Photosynth. Res. 138, 361–371 (2018).
pubmed: 30117121
pmcid: 6244799
doi: 10.1007/s11120-018-0566-0
Wang, F. et al. The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell 32, 3124–3138 (2020).
pubmed: 32796126
pmcid: 7534462
doi: 10.1105/tpc.20.00289
Karim, S. & Aronsson, H. The puzzle of chloroplast vesicle transport – involvement of GTPases. Front. Plant Sci. 5, 472 (2014).
pubmed: 25295043
pmcid: 4171996
doi: 10.3389/fpls.2014.00472
Yang, C. et al. Light-induced rice1 regulates light-dependent attachment of leaf-type ferredoxin-nadp+ oxidoreductase to the thylakoid membrane in rice and Arabidopsis. Plant Cell 28, 712–728 (2016).
pubmed: 26941088
pmcid: 4826015
doi: 10.1105/tpc.15.01027
Park, S. Y. et al. The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649–1664 (2007).
pubmed: 17513504
pmcid: 1913741
doi: 10.1105/tpc.106.044891
Zhang, S. S. et al. Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol. Plant 10, 1004–1006 (2017).
pubmed: 28286297
doi: 10.1016/j.molp.2017.02.007
Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M. & Miyawaki, A. Expanded dynamic range of fluorescent indicators for Ca
pubmed: 15247428
pmcid: 490022
doi: 10.1073/pnas.0400417101
Izumi, M. et al. Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation. Plant Physiol. 167, 1307–1320 (2015).
pubmed: 25717038
pmcid: 4378162
doi: 10.1104/pp.114.254078
Jang, I. C., Nahm, B. H. & Kim, J. K. Subcellular targeting of green fluorescent protein to plastids in transgenic rice plants provides a high-level expression system. Mol. Breed. 5, 453–461 (1999).
doi: 10.1023/A:1009665314850
Kalderon, D., Richardson, W. D., Markham, A. F. & Smith, A. E. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 311, 33–38 (1984).
pubmed: 6088992
doi: 10.1038/311033a0
Wen, W., Meinkoth, J. L., Tsien, R. Y. & Taylor, S. S. Identification of a signal for rapid export of proteins from the nucleus. Cell 82, 463–473 (1995).
pubmed: 7634336
doi: 10.1016/0092-8674(95)90435-2
Pantoja, O. Recent advances in the physiology of ion channels in plants. Annu. Rev. Plant Biol. 72, 463–495 (2021).
pubmed: 33428476
doi: 10.1146/annurev-arplant-081519-035925
Kleist, T. J. & Wudick, M. M. Shaping up: Recent advances in the study of plant calcium channels. Curr. Opin. Cell Biol. 76, 102080 (2022).
pubmed: 35430425
doi: 10.1016/j.ceb.2022.102080
Schägger, H., Cramer, W. A. & von Jagow, G. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220–230 (1994).
pubmed: 8203750
doi: 10.1006/abio.1994.1112
Gilliham, M. et al. Calcium delivery and storage in plant leaves: exploring the link with water flow. J. Exp. Bot. 62, 2233–2250 (2011).
pubmed: 21511913
doi: 10.1093/jxb/err111
Shigeto, J. & Tsutsumi, Y. Diverse functions and reactions of class III peroxidases. New Phytol. 209, 1395–1402 (2016).
pubmed: 26542837
doi: 10.1111/nph.13738
Zhang, Z. et al. Association-dissociation of glycolate oxidase with catalase in rice: A potential switch to modulate intracellular H
pubmed: 26900141
doi: 10.1016/j.molp.2016.02.002
Wong, H. L. et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022–4034 (2007).
pubmed: 18156215
pmcid: 2217649
doi: 10.1105/tpc.107.055624
Suzuki, N. et al. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14, 691–699 (2011).
pubmed: 21862390
doi: 10.1016/j.pbi.2011.07.014
Zhao, H. et al. An inferred functional impact map of genetic variants in rice. Mol. Plant 14, 1584–1599 (2021).
pubmed: 34214659
doi: 10.1016/j.molp.2021.06.025
Pinson, S. R. M. et al. Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Sci. 55, 294–311 (2015).
doi: 10.2135/cropsci2013.10.0656
Gao, M. et al. Ca
pubmed: 34597584
doi: 10.1016/j.cell.2021.09.009
Astegno, A., La Verde, V., Marino, V., Dell’Orco, D. & Dominici, P. Biochemical and biophysical characterization of a plant calmodulin: Role of the N- and C-lobes in calcium binding, conformational change, and target interaction. BBA-Proteins Proteom 1864, 297–307 (2016).
doi: 10.1016/j.bbapap.2015.12.003
Gifford, J. L., Jamshidiha, M., Mo, J., Ishida, H. & Vogel, H. J. Comparing the calcium binding abilities of two soybean calmodulins: towards understanding the divergent nature of plant calmodulins. Plant Cell 25, 4512–4524 (2013).
pubmed: 24254124
pmcid: 3875733
doi: 10.1105/tpc.113.113183
Vallone, R. et al. Metal binding affinity and structural properties of calmodulin-like protein 14 from Arabidopsis thaliana. Protein Sci. 25, 1461–1471 (2016).
pubmed: 27124620
pmcid: 4972202
doi: 10.1002/pro.2942
Zeb, Q. et al. The interaction of CaM7 and CNGC14 regulates root hair growth in Arabidopsis. J. Integr. Plant Biol. 62, 887–896 (2020).
pubmed: 31755194
doi: 10.1111/jipb.12890
Tang, R. J. & Luan, S. Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr. Opin. Plant Biol. 39, 97–105 (2017).
pubmed: 28709026
doi: 10.1016/j.pbi.2017.06.009
Kühlbrandt, W. Biology, structure and mechanism of P-type ATPases. Nat. Rev. Mol. Cell Biol. 5, 282–295 (2004).
pubmed: 15071553
doi: 10.1038/nrm1354
Bi, G. Z. et al. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184, 3528–3541 (2021).
pubmed: 33984278
doi: 10.1016/j.cell.2021.05.003
Wang, J. Z. et al. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, 44–55 (2019).
doi: 10.1126/science.aav5870
Förderer, A. et al. A wheat resistosome defines common principles of immune receptor channels. Nature 610, 532–539 (2022).
pubmed: 36163289
pmcid: 9581773
doi: 10.1038/s41586-022-05231-w
Jacob, P. et al. Plant “helper” immune receptors are Ca
pubmed: 34140391
pmcid: 8939002
doi: 10.1126/science.abg7917
Wang, Z. Q. et al. Plasma membrane association and resistosome formation of plant helper immune receptors. Proc. Natl. Acad. Sci. USA 120, e2222036120 (2023).
pubmed: 37523563
pmcid: 10410763
doi: 10.1073/pnas.2222036120
White, P. J. & Broadley, M. R. Calcium in plants. Ann. Bot. 92, 487–511 (2003).
pubmed: 12933363
pmcid: 4243668
doi: 10.1093/aob/mcg164
Rocha, A. G. & Vothknecht, U. C. The role of calcium in chloroplasts—an intriguing and unresolved puzzle. Protoplasma 249, 957–966 (2012).
pubmed: 22227834
doi: 10.1007/s00709-011-0373-3
Hochmal, A. K., Schulze, S., Trompelt, K. & Hippler, M. Calcium-dependent regulation of photosynthesis. Biochim. Biophys. Acta 1847, 993–1003 (2015).
pubmed: 25687895
doi: 10.1016/j.bbabio.2015.02.010
Conn, S. & Gilliham, M. Comparative physiology of elemental distributions in plants. Ann. Bot. 105, 1081–1102 (2010).
pubmed: 20410048
pmcid: 2887064
doi: 10.1093/aob/mcq027
Yamaji, N. & Ma, J. F. The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci. 19, 556–563 (2014).
pubmed: 24953837
doi: 10.1016/j.tplants.2014.05.007
Sierla, M., Waszczak, C., Vahisalu, T. & Kangasjarvi, J. Reactive oxygen species in the regulation of stomatal movements. Plant Physiol. 171, 1569–1580 (2016).
pubmed: 27208297
pmcid: 4936562
doi: 10.1104/pp.16.00328
Song, Y. W., Miao, Y. C. & Song, C. P. Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 201, 1121–1140 (2014).
pubmed: 24188383
doi: 10.1111/nph.12565
Nomura, H., Komori, T., Kobori, M., Nakahira, Y. & Shiina, T. Evidence for chloroplast control of external Ca
pubmed: 18088326
doi: 10.1111/j.1365-313X.2007.03390.x
Weinl, S. et al. A plastid protein crucial for Ca
pubmed: 18507772
doi: 10.1111/j.1469-8137.2008.02492.x
Huang, X. Y. et al. Natural variation in a molybdate transporter controls grain molybdenum concentration in rice. New Phytol. 221, 1983–1997 (2019).
pubmed: 30339276
doi: 10.1111/nph.15546
Ma, X. et al. A Robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284 (2015).
pubmed: 25917172
doi: 10.1016/j.molp.2015.04.007
Broman, K. W., Wu, H., Sen, S. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890 (2003).
pubmed: 12724300
doi: 10.1093/bioinformatics/btg112
Hu, D., Li, M., Zhao, F. J. & Huang, X. Y. The vacuolar molybdate transporter OsMOT1;2 controls molybdenum remobilization in rice. Front. Plant Sci. 13, 863816 (2022).
pubmed: 35356108
pmcid: 8959823
doi: 10.3389/fpls.2022.863816
Huang, X. Y. et al. A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev. 23, 1805–1817 (2009).
pubmed: 19651988
pmcid: 2720257
doi: 10.1101/gad.1812409
Zhang, H. et al. A genetic module at one locus in rice protects chloroplasts to enhance thermotolerance. Science 376, 1293–1300 (2022).
pubmed: 35709289
doi: 10.1126/science.abo5721
Gualberto, J. M., Handa, H. & Grienenberger, J. M. Isolation and fractionation of plant mitochondria and chloroplasts: specific examples. Methods Cell Biol. 50, 161–175 (1995).
pubmed: 8531792
doi: 10.1016/S0091-679X(08)61029-8
Qian, D., Chen, G., Tian, L. & Qu, L. Q. OsDER1 is an ER-associated protein degradation factor that responds to ER stress. Plant Physiol. 178, 402–412 (2018).
pubmed: 30026288
pmcid: 6130045
doi: 10.1104/pp.18.00375
Chu C. C., Li H. M. Determining the location of an arabidopsis chloroplast protein using in vitro import followed by fractionation and alkaline extraction. In: Jarvis R. P., ed. Chloroplast Research in Arabidopsis: Methods and Protocols, Volume I. Totowa, NJ: Humana Press, 339–350 (2011).
Cunningham, K. W. & Fink, G. R. Calcineurin inhibits VCX1-dependent H
pubmed: 8628289
pmcid: 231210
doi: 10.1128/MCB.16.5.2226
Verkhovskaya, M. Preparation of everted membrane vesicles from Escherichia coli cells. Bio. Protoc. 7, e2254 (2017).
pubmed: 34541243
pmcid: 8410345
doi: 10.21769/BioProtoc.2254
Walter, M. et al. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428–438 (2004).
pubmed: 15469500
doi: 10.1111/j.1365-313X.2004.02219.x
Waadt, R. et al. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505–516 (2008).
pubmed: 18643980
doi: 10.1111/j.1365-313X.2008.03612.x
Zhao, H. et al. RiceVarMap: a comprehensive database of rice genomic variations. Nucleic Acids Res. 43, D1018–D1022 (2015).
pubmed: 25274737
doi: 10.1093/nar/gku894