دورية أكاديمية

Osmosensor-mediated control of Ca 2+ spiking in pollen germination.

التفاصيل البيبلوغرافية
العنوان: Osmosensor-mediated control of Ca 2+ spiking in pollen germination.
المؤلفون: Pei S; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China.; Department of Biology, Duke University, Durham, NC, USA.; Fitzpatrick Institute for Photonics, Duke University, Durham, NC, USA.; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Tao Q; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Li W; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Qi G; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Wang B; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Wang Y; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China., Dai S; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China., Shen Q; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Wang X; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Wu X; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Xu S; Department of Biology, Duke University, Durham, NC, USA., Theprungsirikul L; Department of Biology, Duke University, Durham, NC, USA., Zhang J; Department of Biology, Duke University, Durham, NC, USA., Liang L; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Liu Y; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Chen K; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Shen Y; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Crawford BM; Fitzpatrick Institute for Photonics, Duke University, Durham, NC, USA., Cheng M; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Zhang Q; College of Life Sciences, Zhejiang University, Hangzhou, China.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Wang Y; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Liu H; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Yang B; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China., Krichilsky B; Department of Biology, Duke University, Durham, NC, USA., Pei J; Department of Biology, Duke University, Durham, NC, USA.; Fuqua School of Business, Duke University, Durham, NC, USA., Song K; Department of Biology, Duke University, Durham, NC, USA., Johnson DM; Department of Physics, Duke University, Durham, NC, USA., Jiang Z; Department of Biology, Duke University, Durham, NC, USA., Wu F; Department of Biology, Duke University, Durham, NC, USA., Swift GB; Department of Physics, Duke University, Durham, NC, USA., Yang H; Department of Biochemistry, Duke University, Durham, NC, USA., Liu Z; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China., Zou X; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China., Vo-Dinh T; Fitzpatrick Institute for Photonics, Duke University, Durham, NC, USA., Liu F; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China. jwszjx@hunau.edu.cn.; Department of Biology, Duke University, Durham, NC, USA. jwszjx@hunau.edu.cn., Pei ZM; Department of Biology, Duke University, Durham, NC, USA. zpei@duke.edu.; Fitzpatrick Institute for Photonics, Duke University, Durham, NC, USA. zpei@duke.edu., Yuan F; College of Horticulture and Landscape, Hunan Agricultural University, Changsha, China. yuanfang800@yahoo.com.; Department of Biology, Duke University, Durham, NC, USA. yuanfang800@yahoo.com.; College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China. yuanfang800@yahoo.com.
المصدر: Nature [Nature] 2024 May; Vol. 629 (8014), pp. 1118-1125. Date of Electronic Publication: 2024 May 22.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
أسماء مطبوعة: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
مواضيع طبية MeSH: Arabidopsis*/metabolism , Arabidopsis*/genetics , Calcium*/metabolism , Calcium Signaling* , Germination*/genetics , Osmolar Concentration* , Pollen*/genetics , Pollen*/metabolism, Arabidopsis Proteins/metabolism ; Arabidopsis Proteins/genetics ; Calcium Channels/genetics ; Calcium Channels/metabolism ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Mutation ; Water/metabolism ; HEK293 Cells ; Humans ; Dehydration
مستخلص: Higher plants survive terrestrial water deficiency and fluctuation by arresting cellular activities (dehydration) and resuscitating processes (rehydration). However, how plants monitor water availability during rehydration is unknown. Although increases in hypo-osmolarity-induced cytosolic Ca 2+ concentration (HOSCA) have long been postulated to be the mechanism for sensing hypo-osmolarity in rehydration 1,2 , the molecular basis remains unknown. Because osmolarity triggers membrane tension and the osmosensing specificity of osmosensing channels can only be determined in vivo 3-5 , these channels have been classified as a subtype of mechanosensors. Here we identify bona fide cell surface hypo-osmosensors in Arabidopsis and find that pollen Ca 2+ spiking is controlled directly by water through these hypo-osmosensors-that is, Ca 2+ spiking is the second messenger for water status. We developed a functional expression screen in Escherichia coli for hypo-osmosensitive channels and identified OSCA2.1, a member of the hyperosmolarity-gated calcium-permeable channel (OSCA) family of proteins 6 . We screened single and high-order OSCA mutants, and observed that the osca2.1/osca2.2 double-knockout mutant was impaired in pollen germination and HOSCA. OSCA2.1 and OSCA2.2 function as hypo-osmosensitive Ca 2+ -permeable channels in planta and in HEK293 cells. Decreasing osmolarity of the medium enhanced pollen Ca 2+ oscillations, which were mediated by OSCA2.1 and OSCA2.2 and required for germination. OSCA2.1 and OSCA2.2 convert extracellular water status into Ca 2+ spiking in pollen and may serve as essential hypo-osmosensors for tracking rehydration in plants.
(© 2024. The Author(s).)
References: Hetherington, A. M. & Brownlee, C. The generation of Ca 2+ signals in plants. Annu. Rev. Plant Biol. 55, 401–427 (2004). (PMID: 15377226)
Tazawa, M., Shimmen, T. & Mimura, T. Membrane control in the Characeae. Annu. Rev. Plant Physiol. 38, 95–117 (1987).
Kung, C. A possible unifying principle for mechanosensation. Nature 436, 647–654 (2005). (PMID: 16079835)
Arnadottir, J. & Chalfie, M. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111–137 (2010). (PMID: 20192782)
Kefauver, J. M., Ward, A. B. & Patapoutian, A. Discoveries in structure and physiology of mechanically activated ion channels. Nature 587, 567–576 (2020). (PMID: 332397948477435)
Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca 2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014). (PMID: 25162526)
Hsiao, T. C. Plant responses to water stress. Annu. Rev. Plant Physiol. 24, 519–570 (1973).
Oliver, M. J. et al. Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annu. Rev. Plant Biol. 71, 435–460 (2020). (PMID: 32040342)
Johnson, M. A., Harper, J. F. & Palanivelu, R. A fruitful journey: pollen tube navigation from germination to fertilization. Annu. Rev. Plant Biol. 70, 809–837 (2019). (PMID: 30822112)
Kim, Y. J., Zhang, D. B. & Jung, K. H. Molecular basis of pollen germination in cereals. Trends Plant Sci. 24, 1126–1136 (2019). (PMID: 31610991)
Bremer, E. & Kramer, R. Responses of microorganisms to osmotic stress. Annu. Rev. Microbiol. 73, 313–334 (2019). (PMID: 31180805)
Bourque, C. W. Central mechanisms of osmosensation and systemic osmoregulation. Nat. Rev. Neurosci. 9, 519–531 (2008). (PMID: 18509340)
Waadt, R. et al. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 23, 680–694 (2022). (PMID: 355137179592120)
Zhang, H., Zhu, J., Gong, Z. & Zhu, J.-K. Abiotic stress responses in plants. Nat. Rev. Genet. 23, 104–119 (2022). (PMID: 34561623)
Okazaki, Y., Yoshimoto, Y., Hiramoto, Y. & Tazawa, M. Turgor regulation and cytoplasmic free Ca 2+ in the alga Lamprothamnium. Protoplasma 140, 67–71 (1987).
Taylor, A. R., Manison, N. F. H., Fernandez, C., Wood, J. & Brownlee, C. Spatial organization of calcium signaling involved in cell volume control in the fucus rhizoid. Plant Cell 8, 2015–2031 (1996). (PMID: 12239374161331)
Bickerton, P., Sello, S., Brownlee, C., Pittman, J. K. & Wheeler, G. L. Spatial and temporal specificity of Ca 2+ signalling in Chlarnydomonas reinhardtii in response to osmotic stress. New Phytol. 212, 920–933 (2016). (PMID: 275160455111745)
Takahashi, K., Isobe, M., Knight, M. R., Trewavas, A. J. & Muto, S. hypo-osmotic shock induces increases in cytosolic Ca 2+ in tobacco suspension-culture cells. Plant Physiol. 113, 587–594 (1997). (PMID: 12223627158174)
Kudla, J. et al. Advances and current challenges in calcium signaling. New Phytol. 218, 414–431 (2018). (PMID: 29332310)
Hedrich, R. Ion channels in plants. Physiol. Rev. 92, 1777–1811 (2012). (PMID: 23073631)
Zipfel, C. & Oldroyd, G. E. D. Plant signalling in symbiosis and immunity. Nature 543, 328–336 (2017). (PMID: 28300100)
Liedtke, W. et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103, 525–535 (2000). (PMID: 110816382211528)
Julius, D. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29, 355–384 (2013). (PMID: 24099085)
Jiang, Z. et al. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca 2+ influx. Nature 572, 341–346 (2019). (PMID: 31367039)
Wu, F. H. et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581 (2020). (PMID: 32076270)
Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343, 290–294 (2014). (PMID: 24436418)
Laohavisit, A. et al. Quinone perception in plants via leucine-rich-repeat receptor-like kinases. Nature 587, 92–97 (2020). (PMID: 32879491)
Kutschera, A. et al. Bacterial media-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364, 178–181 (2019). (PMID: 30975887)
Zhang, M. F. et al. Structure of the mechanosensitive OSCA channels. Nat. Struct. Mol. Biol. 25, 850–858 (2018). (PMID: 30190597)
Thor, K. et al. The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity. Nature 585, 569–573 (2020). (PMID: 328464268435934)
Liu, X., Wang, J. W. & Sun, L. F. Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2. Nat. Commun. 9, 9 (2018).
Jojoa-Cruz, S. et al. Cryo-EM structure of the mechanically activated ion channel OSCA1.2. eLife 7, e41845 (2018). (PMID: 303829396235563)
Hamilton, E. S., Schlegel, A. M. & Haswell, E. S. United in diversity: mechanosensitive ion channels in plants. Annu. Rev. Plant Biol. 66, 113–137 (2015). (PMID: 25494462)
Venkatachalam, K. & Montell, C. TRP channels. Annu. Rev. Biochem. 76, 387–417 (2007). (PMID: 175795624196875)
Wu, X. M., Yuan, F., Wang, X. W., Zhu, S. & Pei, Z.-M. Evolution of osmosensing OSCA1 Ca 2+ channel family coincident with plant transition from water to land. Plant Genome 15, e20198 (2022). (PMID: 35502648)
Radin, I. et al. Plant PIEZO homologs modulate vacuole morphology during tip growth. Science 373, 586–590 (2021). (PMID: 34326243)
Mousavi, S. A. R. et al. PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 118, e2102188118 (2021). (PMID: 339759578158017)
Yoshimura, K., Iida, K. & Iida, H. MCAs in Arabidopsis are Ca 2+ -permeable mechanosensitive channels inherently sensitive to membrane tension. Nat. Commun. 12, 6074 (2021). (PMID: 346671738526687)
Levina, N. et al. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18, 1730–1737 (1999). (PMID: 102021371171259)
Rosano, G. L. & Ceccarelli, E. A. Recombinant protein expression in Escherichia coli: advances and challenges. Front. Microbiol. 5, 172 (2014). (PMID: 248605554029002)
Hepler, P. K., Kunkel, J. G., Rounds, C. M. & Winship, L. J. Calcium entry into pollen tubes. Trends Plant Sci. 17, 32–38 (2012). (PMID: 22104406)
Brewbake, J. L. & Kwack, B. H. Essential role of calcium ion in pollen germination and pollen tube growth. Am. J. Bot. 50, 859–865 (1963).
Cheung, A. Y. & Wu, H. M. Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu. Rev. Plant Biol. 59, 547–572 (2008). (PMID: 18444907)
Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013). (PMID: 238682583777791)
Hamilton, E. S. et al. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350, 438–441 (2015). (PMID: 264947584764502)
Clapham, D. E. TRP channels as cellular sensors. Nature 426, 517–524 (2003). (PMID: 14654832)
Iwano, M. et al. Ca 2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol. 136, 3562–3571 (2004). (PMID: 15489279527155)
Diao, M., Qu, X. L. & Huang, S. J. Calcium imaging in Arabidopsis pollen cells using G-CaMP5. J. Integr. Plant Biol. 60, 897–906 (2018). (PMID: 29424471)
Wudick, M. M. et al. CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca 2+ homeostasis. Science 360, 533–536 (2018). (PMID: 29724955)
Frietsch, S. et al. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc. Natl Acad. Sci. USA 104, 14531–14536 (2007). (PMID: 177261111964830)
Nichols, R. J. et al. Phenotypic landscape of a bacterial cell. Cell 144, 143–156 (2011). (PMID: 21185072)
Ali, R., Zielinski, R. E. & Berkowitz, G. A. Expression of plant cyclic nucleotide-gated cation channels in yeast. J. Exp. Bot. 57, 125–138 (2006). (PMID: 16317039)
Kung, C., Martinac, B. & Sukharev, S. Mechanosensitive channels in microbes. Annu. Rev. Microbiol. 64, 313–329 (2010). (PMID: 20825352)
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012). (PMID: 229308345554542)
Zonia, L. & Munnik, T. Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol. 134, 813–823 (2004). (PMID: 14739344344556)
Michard, E. et al. Glutamate receptor–like genes form Ca 2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332, 434–437 (2011). (PMID: 21415319)
Zhang, J. et al. Sperm cells are passive cargo of the pollen tube in plant fertilization. Nat. Plants 3, 17079 (2017). (PMID: 285855625960590)
Steinhorst, L. et al. Vacuolar CBL-CIPK12 Ca 2+ -sensor-kinase complexes are required for polarized pollen tube growth. Curr. Biol. 25, 1475–1482 (2015). (PMID: 25936548)
Zonia, L., Müller, M. & Munnik, T. Hydrodynamics and cell volume oscillations in the pollen tube apical region are integral components of the biomechanics of Nicotiana tabacum pollen tube growth. Cell Biochem. Biophys. 46, 209–232 (2006). (PMID: 17272849)
Li, H. J., Meng, J. G. & Yang, W. C. Multilayered signaling pathways for pollen tube growth and guidance. Plant Reprod. 31, 31–41 (2018). (PMID: 29441420)
Li, H., Lin, Y., Heath, R. M., Zhu, M. X. & Yang, Z. Control of pollen tube tip growth by a Rop GTPase–dependent pathway that leads to tip-localized calcium influx. Plant Cell 11, 1731–1742 (1999). (PMID: 10488239144310)
Jacob, P. et al. Plant “helper” immune receptors are Ca 2+ -permeable nonselective cation channels. Science 373, 420–425 (2021). (PMID: 341403918939002)
Cheung, A. Y., Boavida, L. C., Aggarwal, M., Wu, H. M. & Feijo, J. A. The pollen tube journey in the pistil and imaging the in vivo process by two-photon microscopy. J. Exp. Bot. 61, 1907–1915 (2010). (PMID: 20363865)
Huang, J. B. et al. Stigma receptors control intraspecies and interspecies barriers in Brassicaceae. Nature 614, 303–308 (2023). (PMID: 366978259908550)
Zhang, L. L. et al. FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa. Curr. Biol. 31, 3004–U3072 (2021). (PMID: 34015250)
Caterina, M. J. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824 (1997). (PMID: 9349813)
Han, S. C., Tang, R. H., Anderson, L. K., Woerner, T. E. & Pei, Z.-M. A cell surface receptor mediates extracellular Ca 2+ sensing in guard cells. Nature 425, 196–200 (2003). (PMID: 12968184)
Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55–60 (2010). (PMID: 208139203062430)
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998). (PMID: 10069079)
Cheung, A. Y. & Wu, H.-M. Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16, 257–269 (2004). (PMID: 14671023301409)
de Graaf, B. H. J. et al. Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17, 2564–2579 (2005). (PMID: 161003361197435)
Meng, J. G. et al. Integration of ovular signals and exocytosis of a Ca 2+ channel by MLOs in pollen tube guidance. Nat. Plants 6, 143–154 (2020). (PMID: 32055051)
Bolte, S. et al. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214, 159–173 (2004). (PMID: 15102063)
Hooper, C. M., Castleden, I. R., Tanz, S. K., Aryamanesh, N. & Millar, A. H. SUBA4: the interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Res. 45, D1064–D1074 (2017). (PMID: 27899614)
Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987). (PMID: 3327686553867)
Zhong, S. et al. Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis. Science 364, 851 (2019).
Mecchia, M. A. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600–1603 (2017). (PMID: 29242232)
Monshausen, G. B., Bibikova, T. N., Weisenseel, M. H. & Gilroy, S. Ca 2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21, 2341–2356 (2009). (PMID: 196542642751959)
Denninger, P. et al. Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat. Commun. 5, 4645 (2014). (PMID: 25145880)
Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018). (PMID: 30213912)
Damineli, D. S. C., Portes, M. T. & Feijo, J. A. Oscillatory signatures underlie growth regimes in Arabidopsis pollen tubes: computational methods to estimate tip location, periodicity, and synchronization in growing cells. J. Exp. Bot. 68, 3267–3281 (2017). (PMID: 283696035853864)
Guo, J., He, J., Dehesh, K., Cui, X. & Yang, Z. CamelliA-based simultaneous imaging of Ca 2+ dynamics in subcellular compartments. Plant Physiol. 188, 2253–2271 (2022). (PMID: 352183528968278)
Ruiz, M. C. M. et al. Circadian oscillations of cytosolic free calcium regulate the Arabidopsis circadian clock. Nat. Plants 4, 690–698 (2018). (PMID: 6152895)
Basu, D. & Haswell, E. S. The mechanosensitive ion channel MSL10 potentiates responses to cell swelling in Arabidopsis seedlings. Curr. Biol. 30, 2716–2728 (2020). (PMID: 32531281)
Morgan, J. M. Osmoregulation and water-stress in higher-plants. Annu. Rev. Plant Physiol. 35, 299–319 (1984).
Munns, R. & Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant. Biol. 59, 651–681 (2008). (PMID: 18444910)
Maggio, A., Zhu, J.-K., Hasegawa, P. M. & Bressan, R. A. Osmogenetics: aristotle to Arabidopsis. Plant Cell 18, 1542–1557 (2006). (PMID: 168098141488915)
Wang, Z.-Y. & Tobin, E. M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217 (1998). (PMID: 9657153)
Newton, A. C., Bootman, M. D. & Scott, J. D. Second messengers. Cold Spring Harbor Perspect. Biol. 8, a005926 (2016).
Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517–529 (2003). (PMID: 12838335)
Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E. D. & Schroeder, J. I. Genetic strategies for improving crop yields. Nature 575, 109–118 (2019). (PMID: 316952057024682)
Yu, X., Feng, B., He, P. & Shan, L. From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 55, 109–137 (2017). (PMID: 285253096240913)
Edel, K. H., Marchadier, E., Brownlee, C., Kudla, J. & Hetherington, A. M. The evolution of calcium-based signalling in plants. Curr. Biol. 27, R667–R679 (2017). (PMID: 28697370)
Oldroyd, G. E. D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013). (PMID: 23493145)
Helliwell, K. E. et al. Spatiotemporal patterns of intracellular Ca 2+ signalling govern hypo-osmotic stress resilience in marine diatoms. New Phytol. 230, 155–170 (2021). (PMID: 33486789)
المشرفين على المادة: 0 (Arabidopsis Proteins)
SY7Q814VUP (Calcium)
0 (Calcium Channels)
059QF0KO0R (Water)
تواريخ الأحداث: Date Created: 20240522 Date Completed: 20240530 Latest Revision: 20240601
رمز التحديث: 20240602
مُعرف محوري في PubMed: PMC11136663
DOI: 10.1038/s41586-024-07445-6
PMID: 38778102
قاعدة البيانات: MEDLINE
الوصف
تدمد:1476-4687
DOI:10.1038/s41586-024-07445-6