Skip to main content
SpringerLink
Log in

Distribution and Functions of Calcium Mineral Deposits in Photosynthetic Organisms

  • Chapter
  • First Online:
Progress in Botany Vol. 84

Part of the book series: Progress in Botany ((BOTANY,volume 84))

  • 134 Accesses

Abstract

CaCO3 precipitates occur inside a few cyanobacteria and green algae. More common is precipitation on the surface of cyanobacteria, a range of algae and aquatic plants, and in invaginations of the cell wall in terrestrial plants (cystoliths). In coccolithophores and calcified dinoflagellates, CaCO3 is precipitated with organic matter in intracellular vesicles and the resulting structures are externalised. The precipitation of CaCO3 on the surface of photosynthesising structures is related to the consumption of CO2 in photosynthesis. CO2 production by root respiration can solubilise soil CaCO3. A few cyanobacteria and eukaryotic algae can bore through solid CaCO3 by removing Ca2+ and adding H+ at the site of boring, generating soluble inorganic C that can be used in photosynthesis. Ca(COO)2 is precipitated in the vacuoles of many algae and plants, and the cell walls of some plants.

An outcome of precipitation of CaCO3 using CO3= produced from CO2, and Ca2+, is the production of H+; the same is the case for precipitation of Ca(COO)2 from (COOH)2 and Ca2+. The H+ produced by Ca(COO2) can be used to neutralise OH− produced in NO3− assimilation in the shoot without increasing cell osmolarity. There is no evidence of CaCO3 fulfilling this role. Another outcome of CaCO3 and Ca(COO)2 precipitation is Ca2+ immobilisation, though with little evidence of remobilisation of Ca2+ under Ca2+ deficiency. Other consequences of CaCO3 and Ca(COO)2 precipitation are light scattering and increased density, and ‘alarm photosynthesis’. Defence against herbivores and pathogens is better established for Ca(COO)2 than for CaCO3, and pollen release from anthers is a function of Ca(COO)2 but not CaCO3.

Communicated by Ulrich Lüttge

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adey W, Halfar J, Humpheys A, Suskiewicz T, Delanger D, Gagnon P, Fox M (2015) Subarctic rhodolith beds promote longevity of crustose coralline algal buildups and their climate archive potential. Palaios 30:281–203

    Google Scholar 

  • Aggarwal SG, Kawamura K (2008) Molecular distributions and stable isotopic compositions of dicarboxylic acids and stable carbon isotopic composition of dicarboxylic acids and related compounds in aerosols from Sapporo, Japan: implication for photochemical aging during long-range atmospheric transport. J Geophys Res 113. article D14

    Google Scholar 

  • Aggarwal SG, Kawamura K (2008) Molecular distribution and stable carbon isotope compositions of dicarboxylic acids in aerosols from Sapporo, Japan: atmospheric transport. J Geophys Res 113:D14301

    Google Scholar 

  • Ajello L (1941) Cytology and cellular interrelations of cystolith formation in Ficus elastica. Am J Bot 28:589–594

    Google Scholar 

  • Akpan EB, Farrow GE (1984) Shell-boring algae on the Scottish continental shelf: identification, distribution, bathymetric zonation. Earth Env Trans R Soc Edin 75:1–12

    Google Scholar 

  • Al Daini H, Norman HC, Young P, Barrett-Lennard EG (2013) The source of nitrogen (NH4+ or NO3−) affects the concentration of oxalate in the shoot and growth of Atriplex nummularia (oldman saltbush). Funct Plant Biol 40:1057–1064

    PubMed  Google Scholar 

  • Aloisi G (2008) The calcium carbonate saturation state in cyanobacterial mats throughout Earth’s history. Geochim Cosmochim Acta 72:6037–6060

    Google Scholar 

  • Anthoons B (2017) Distribution of calcium oxalate crystals in ferns and lycophytes. MSc thesis, Ghent University, Belgium

    Google Scholar 

  • Balch WM (2018) The ecology, biogeochemistry, and optical properties of coccolithophores. Ann Rev Mar Sci 9:283–310

    Google Scholar 

  • Balch WM, Holligan PM, Ackleson SG, Voss KJ (1991) Biological and optical properties of mesoscale coccolithophore blooms in the Gulf of Maine. Limnol Oceanogr 36:629–643

    Google Scholar 

  • Bauer M, Meyer AJ, Heumann H-G, Lützelschwab M, Michalke W (1996) Distribution of plasma membrane H+-ATPase and polar current patterns of Elodea canadensis. Bot Acta 109:382–387

    Google Scholar 

  • Beazley MJ, Rickman RD, Ingram DK, Boutton TW, Russ J (2002) The natural abundance of carbon isotopes (14C, 13C) in lichens and calcium carbonate pruina: implications for archaeological and palaeoenvironmental studies. Radiocarbon 44:675–683

    Google Scholar 

  • Beilby MJ, Casanova MT (2014) The physiology of characean cells. Springer, Berlin, p 194

    Google Scholar 

  • Benzecry A, Brack-Hanes SD (2008) A new hydrocharitacean seagrass for the Eocene of Florida. Bot J Linn Soc 157:19–30

    Google Scholar 

  • Benzerara K, Skouri-Panet F, Férard C, Gugger M, Laurent T, Coutadeau E, Ragon M, Cosmidis J, Mengug N, Margaret-Oliver I, Tavera R, López-García P, Moreira D (2014) Intracellular Ca-carbonate biomineralisation is widespread in cyanobacteria. Proc Natl Acad Sci U S A 111:10933–10938

    PubMed  PubMed Central  Google Scholar 

  • Benzerara K, Duprat E, Bitard-Feildel T, Gaumes G, Casser-Chauvet G, Chauvet F, Dezi M, Dion SI, Gaschignard G, Görgen S, Gogger M, López-Garcia P, Millet M, Skouri-Panet F, Moreira D, Collebaut I (2022) A new gene family diagnostic for intracellular biomineralisation of amorphous Ca carbonates by cyanobacteria. Genome Biol Evol 14(3):evac026. https://doi.org/10.1093/gbe/evac026

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernardino-Nicanor A, Teniente-Martinez G, Juarez-Goiz JMS, Filardo-Kerstupp S, Montañez-Soto JL, González-Cruz L (2012) Changes in the concentration and characteristics of calcium oxalate crystals during development stages of Agave atrovirens. Adv Biores 3:22–28

    Google Scholar 

  • Blondeau M, Sachae M, Boutlonge C, Gillet C, Guigner J-M, Skouri-Panet F, Poinsot C, Ferard C, Miot J, Benzerara K (2018) Amorphous calcium carbonate granules form within an intracellular compartment in calcifying cyanobacteria. Front Microbiol 9. article 1768

    Google Scholar 

  • Borowitzka MA, Larkum AWD, Nockolds CE (1974) A scanning electron microscope study of the structure and organization of the calcium carbonate deposits of algae. Phycologia 13:195–203

    Google Scholar 

  • Bosak T, Knoll AH, Petroff AP (2013) The meaning of stromatolites. Annu Rev Earth Planet Sci 41:21–44

    Google Scholar 

  • Bown P, Young J (2019) The fossil record of coastal coccolithophores. J Nanoplankton Res (sp4):73–80

    Google Scholar 

  • Brack-Hanes SD, Greco AM (1988) Biomineralisation in Thalassia testudinum (Liliopsida, Hydrocharitaceae) and an Eocene seagrass. Trans Am Microsc Soc 107:286–292

    Google Scholar 

  • Bramucci AR, Labeeuw L, Grata FD, Ryan M, Malmstrom RR, Case RJ (2018) The bacterial symbiont Phaeobacter inhibens shapes the life history of its algal host Emiliania huxleyi. Front Mar Sci 5:188

    Google Scholar 

  • Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, White JP (2003) Variation in shoot calcium content in angiosperms. J Exp Bot 54:1431–1446

    PubMed  Google Scholar 

  • Brownlee C, Langer G, Wheeler GL (2021) Coccolithophore calcification: changing paradigms in changing oceans. Acta Biomater 12:4–11

    Google Scholar 

  • Bume RV, Moore LS (1987) Microbialites: organosedimentary deposits of benthic microbial communities. Palaios 2:241–254

    Google Scholar 

  • Campbell SE (1980) Palaeoconchocelis starmachii. a carbonate boring microfossil from the Silurian of Poland (425 million years ago): implications for the evolution of the Bangiaceae (Rhodophyta). Phycologia 19:25–36

    Google Scholar 

  • Canny MJ (1973) Phloem translocation. Cambridge University Press, Cambridge, pp x + 301

    Google Scholar 

  • Canti MG (1997) An investigation of microscopic calcareous spherulites from herbivore dung. J Archaeol Sci 24:219–231

    Google Scholar 

  • Canti MG (1998) The micromorphological identification of faecal spherulites from archaeological and modern materials. J Archaeol Sci 25:435–444

    Google Scholar 

  • Canti MG (1999) The production and preservation of faecal spherulites: animals, environment and taphonomy. J Archaeol Sci 26:251–258

    Google Scholar 

  • Carlquist S (1990) Wood and bark anatomy of the new world species of Ephedra. Alisio J Syst Florist Bot 12:441–483

    Google Scholar 

  • Carlton AG, Turpin BJ, Altieri KE, Seitzinger S, Reff A, Lim H-J, Ervans B (2007) Atmospheric oxalic acid and SOA production from glyoxal: results of aqueous photooxidation experiments. Atmos Environ 41:7588–7602

    Google Scholar 

  • Cavosie A, Silvesterstone J (2003) Early Proterozoic ocean crust in the northern Colorado front range: implications for crustal growth and initiation of basement faults. Tectonics 22. article1015

    Google Scholar 

  • Chareyre MJ (1885) Cystoliths. Nature 32:407

    Google Scholar 

  • Chen J, Sun C, Zhou Q (2013) Direct observation of the bulk and surface chemical morphologies of Ginkgo biloba leaves by Fournier transform mid- and near-infrared microscopic imaging. Anal Bioanal Chem 405:9385–9400

    PubMed  Google Scholar 

  • Cheng S, Xian W, Fu Y, Marin B, Keller J, Wu T, Sun W, Li X, Xu Y, Zhang Y, Wittick S, Reder T, Günther G, Gontcharov A, Wang S, Li L, Liu X, Wang J, Yang H, Xu Y, Delaux PM, Melkonian B, Wang GK-S, Melkonian M (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179:1057–1067.e14

    Google Scholar 

  • Clokie JJP, Boney AD (1980) Conchocelis distribution in the firth of clyde: estimates of the lower limit of the photic zone. J Exp Mar Biol Ecol 46:111–125

    Google Scholar 

  • Coiro M, Lamaga MRB, Rudall PJ (2021) Stomatal development of the family Zamiaceae. Ann Bot 128:555–588

    Google Scholar 

  • Costa A, Navazzio L, Szabo I (2018) The contribution of organelles to plant intracellular calcium signalling. J Exp Bot 69:4175–4193

    Google Scholar 

  • Couradeau E, Benzerara K, Gérard E, Moreira D, Bernard S, Brown GE, López-Garcia P (2012) An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 366:459–462

    Google Scholar 

  • Cramer MD, Hawkins H-J (2009) A physiological mechanism for the formation of root casts. Palaeogeogr Palaeoclimatol Paleoecol 274:125–133

    Google Scholar 

  • Craveiro SC, Pandeirada MS, Daugbjerg N, Moestrup Ø, Calado AJ (2019) Ultrastructure and phylogeny of Theleodinium calcisporum gen. et sp. nov., a freshwater dinoflagellate that produces calcareous cysts. Phycologia 52:488–507

    Google Scholar 

  • Cuellar-Cruz M, Pérez KS, Mendoza ME, Moreno A (2020) Biocrystals in plants: a short review on biomineralisation processes and the role of phototropins into the uptake of calcium. Crystals 10:591

    Google Scholar 

  • Darrenougue N, De Dekker F, Payri C, Eggins S, Fllon F (2013) Growth and chronology of the rhodolith-forming coralline red alga Sporolithon durum. Mar Ecol Prog Ser 474:105–119

    Google Scholar 

  • De Seoane LV (1998) Comparative studies on extant and fossil conifer leaves from the Baqueró formation (Lower Cretaceous), Santa Cruz Province, Argentina. Rev Palaeobot Palynol 99:247–263

    Google Scholar 

  • de Sousa T, Tãneg F, Bass D, de Oliveria A, Figuerido M, Cherchinski A (2014) Deep-water rhodolith bed from the central Brazilian continental shelf, Campos Basin: coralline algae and faunal taxonomic composition. Galaxea J Coral Reef Stud 16:21–31

    Google Scholar 

  • De Wever A, Benzerara K, Coutard M, Gaumes G, Poinsot M, Skouri-panet P, Laurent T, Duprat E, Gugger M (2019) Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO3 and impact on their growth. Geobiology 17:676–690

    PubMed  Google Scholar 

  • DeLucia EH, Nelson K, Vogelmann TC, Smith WK (1996) Contribution of intercellular reflectance to photosynthesis in shade leaves. Plant Cell Environ 19:159–170

    Google Scholar 

  • Durak GM, Taylor AR, Walker CE, Probert I, de Vargas C, Audic S, Schroeder D, Brownlee C, Wheeler GL (2016) A role for diatom-like silicon transporters in calcifying coccolithophores. Nat Commun 7:article 10543

    PubMed  Google Scholar 

  • Durak GM, Brownlee C, Wheeler GL (2017) The role of the cytoskeleton in biomineralisation in haptophyte algae. Sci Rep 7:15409

    PubMed  PubMed Central  Google Scholar 

  • Duthie AV (1912) Anatomy of Gnetum africanum. Ann Bot 26:593–602

    Google Scholar 

  • Elzenga T, Prins HBA (1989) Light-induced polar pH changes in leaves of Elodea Canadensis: 1. Effects of carbon concentration and light intensity. Plant Physiol 91:62–67

    PubMed  PubMed Central  Google Scholar 

  • Emiliani C (1992) Plant earth – cosmology, geology and the evolution of life and environment. Cambridge University Press, Cambridge, p 717

    Google Scholar 

  • Enríquez S, Schubert N (2014) Direct contribution of the seagrass Thalassia testudinum to lime mud production. Nat Commun 5:3835

    PubMed  Google Scholar 

  • Fang M, Tang D, Shi X, Zhou L, Zhou X, Wu M, Song H, Riding R (2022) Early Mesoproterozoic Ca-carbonate precipitates record fluctuations in shallow marine oxygenation. Precambrian Res 373:106630

    Google Scholar 

  • Fankboner PV (1971) Intracellular digestion of symbiontic zooxanthellae by host amoebocytes in giant clams (Bivalvia: Tridacnidae) with a note on the nutritional role of the hypertrophied siphonal epidermis. Biol Bull 141:222–234

    Google Scholar 

  • Fiehn O (2003) Metabolic networks of Cucurbita maxima phloem. Phytochemistry 62:975–886

    Google Scholar 

  • Foster MS, Amado-Filho GM, Kamenos NA, Riosmena-Rodríguez R, Steller DL (2013) Rhodoliths and rhodolith beds. Smithson Contrib Mar Sci 39:143–155

    Google Scholar 

  • Foster J, Luo B, Nakata PA (2016) An oxalyl-CoA dependent pathway of oxalate catabolism plays a role in regulating calcium oxalate crystal accumulation and defending against oxalate-secreting phytopathogens Medicago truncatula. PloS One 11:article e0149850

    PubMed  Google Scholar 

  • Fournier G, Neukermans G (2017) An analytical model of light back-scattering by coccoliths and coccospheres of Emiliania huxleyi. Opt Express 13:14996–15009

    Google Scholar 

  • Frada M, Probert I, Allen MJ, Wilson WH, de Vargas C (2008) The ‘Cheshire Cat’ escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc Natl Acad Sci U S A 105:15944–15949

    PubMed  PubMed Central  Google Scholar 

  • Franceschi VR (1987) Oxalic acid metabolism and calcium oxalate formation in Lemna minor L. Plant Cell Environ 10:397–406

    Google Scholar 

  • Franceschi VR (1989) Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma 148:130–137

    Google Scholar 

  • Franceschi VR, Horner PA (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427

    Google Scholar 

  • Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annu Rev Plant Biol 56:41–71

    PubMed  Google Scholar 

  • Frankignoule M, Canon C, Gattuso JP (1994) Marine calcification as a source of carbon dioxide: positive feedback of increasing atmospheric CO2. Limnol Ocanogr 39:458–468

    Google Scholar 

  • Fredricq S, Krayesky-Self S, Sarvage T, Richards J, Kittle R, Araki N, Hickerson E, Schmidt WE (2019) The critical importance for rhodoliths in the life cycle of both macro- and microalgae, and as holobionts for the establishment and maintenance of biodiversity. Front Mar Sci 5:502

    Google Scholar 

  • Friedmann I, Roth WC, Turner JB, McEwan RS (1977) Calcium oxalate crystals in the green alga Penicillus and related genera. Science 177:891–893

    Google Scholar 

  • Gal A, Hirsch A, Siegel S, Li C, Aichmayer B, Politi Y, Fratzi P, Weiners S, Addadi L (2012a) Plant cystoliths: a complex functional biocomposite of four distinct silicon and amorphous calcium carbonate phases. Chem Eur J 18:10262–10270

    PubMed  Google Scholar 

  • Gal A, Brumfeld V, Weiner S, Addadi L, Oron D (2012b) Certain biominerals in leaves act as light scatterers. Adv Opt Mater 24:OP77–OP83

    Google Scholar 

  • Gal A, Sorrentina A, Kahil K, Pereiro E, Faivre D, Scheffel IA (2018) Nature state image of calcifying and non-calcifying microalgae reveals similarities in their calcium storage organelles. Proc Natl Acad Sci U S A 115:11000–11005

    PubMed  PubMed Central  Google Scholar 

  • Garcia-Pichel F, Ramírez-Reinet E, Gao Q (2010) Microbial excavation of solid carbonates powered by P-type ATPase-mediated transcellular Ca2+ transport. Proc Natl Acad Sci U S A 107:21749–21754

    PubMed  PubMed Central  Google Scholar 

  • Garrett P (1970) Phanerozoic stromatolites: non-competitive ecological restriction by grazing and burrowing animals. Science 169:171–173

    PubMed  Google Scholar 

  • Ghashghaie J, Badeck FW (2014) Opposite carbon isotope discrimination during respiration in leaves versus roots – a review. New Phytol 201:755–769

    Google Scholar 

  • Ghashghaie J, Badeck FW, Girardin C, Huignard C, Aydinlis Z, Fontery C, Priault P, Fresneau G, Lamothe-Sibold M, Strb P, Terwilliger VJ (2016) Changes and their possible causes in δ13C of dark-respired CO2 and its putative bulk and soluble sources during maize ontogeny. J Exp Bot 67:2603–2615

    PubMed  Google Scholar 

  • Gianopoulos A, Nikolopoulos D, Bresta P, Samantas A, Reppa C, Karaboiki K, Dotsika E, Fassseas C, Liakopoulos G, Karabourniotis G (2019) Cystoliths of Parietaria judaica as an internal source of CO2 for photosynthetic assimilation when stomata are closed. J Exp Bot 70:5753–5763

    Google Scholar 

  • Giordano C, Maleci L, Agati G, Petrucelli R (2020) Ficus carica L. leaf anatomy: trichomes and solid inclusions. Ann Appl Biol 176:47–54

    Google Scholar 

  • Giraldo-Ruiz R, Matez P, Bonilla I, Fernandez-Piñas F (1997) The relationship between intracellular pH, growth characteristics and calcium in the cyanobacterium Anabaena sp. strain PCC 7120 exposed to low pH. New Phytol 137:99–105

    Google Scholar 

  • Giraldo-Ruiz R, Bonilla I, Fernandez-Piñas F (1999) Role of external calcium in homeostasis of intracellular pH in the cyanobacterium Anabaena sp. strain PCC 7120 exposed to low pH. New Phytol 141:99–105

    Google Scholar 

  • Gómez-Espínoza O, González-Ramírez D, Bresta P, Karabourniotis G, Bravo LA (2020) Decomposition of calcium oxalate crystals in Colobanthus quitensis under CO2 limiting conditions. MDPI Plants 9:1307

    Google Scholar 

  • Gómez-Espínoza O, González-Ramírez D, Méndez-Goméz J, Guillén-Watson R, Medaglia-Mata A, Bravo LA (2021) Calcium oxalate crystals in leaves of the extremophile plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae). MDPI Plants 10:1787

    Google Scholar 

  • Gordon HR, Smyth TJ, Balch WM, Boynton GC, Tarran GA (2009) Light scattering by coccoliths detached from Emiliania huxleyi. Appl Optics 48:6059–6073

    Google Scholar 

  • Gottschling M, Keupp H, Plötner J, Knop R, Willems H, Kirsch M (2005) Phylogeny of calcareous dinoflagellates as inferred from ITS ribosomal sequence data. Mol Phylogenet Evol 6:444–445

    Google Scholar 

  • Granier B (2012) The contribution of calcareous green algae to the production of limestones. Geodiversitas 34:35–60

    Google Scholar 

  • Grotzinger JP (1990) Geochemical model for Proterozoic stromatolite decline. Am J Sci 290-A:80–103

    Google Scholar 

  • Guenther R, Porcher EMA, Carrington E, Martone PT (2022) Effects of temperature and pH on the growth, calcification and biomechanics on two species of articulated coralline algae. Mar Ecol Prog Ser 700:79–93

    Google Scholar 

  • Guida BS, Garcia-Pichel F (2016) Extreme cellular adaptations for cell differentiation required by a cyanobacterium for carbonate excavation. Proc Natl Acad Sci U S A 113:5712–5717

    PubMed  PubMed Central  Google Scholar 

  • Guida BS, Bose M, Garcia-Pichel F (2017) Carbon fixation from mineral carbonate. Nat Commun 8:1025

    PubMed  PubMed Central  Google Scholar 

  • Gupta VP, Tewari SK, Datta RK (1995) Surface ultrastructural studies on ingress and establishment of Pseudomonas syringae pv. mori on mulberry leaves. J Phytopathol 143:415–418

    Google Scholar 

  • Harpenslager SF, Smolders AJP, Keskamp AAM, Roelefs JGM, Lamers LPM (2015) To float or not to float?: how interactions between light and dissolved inorganic carbon species determine the buoyancy of Stratiotes aloides. PloS One 10:e61249266

    Google Scholar 

  • Hartl WP, Klapper H, Barbier B, Emzikat HJ, Dronkowski R, Müller P, Ostendorp G, Tye A, Bauer R, Barthlott W (2007) Diversity of calcium oxalate crystals in Cactaceae. Can J Bot 85:501–517

    Google Scholar 

  • Hattin DE (1975) Petrology and origin of fecal pellets in upper-cretaceous strata of Kansas and Saskatchewan. J Sediment Petrol 45:686–696

    Google Scholar 

  • He H, Veneklaas EJ, Kuo J, Lambers H (2014) Physiological and ecological significance of biomineralisation in plants. Trends Plant Sci 19:166–174

    PubMed  Google Scholar 

  • Hendry KR, Marron AO, Vincent F, Conley DJ, Gehlen M, Ibarbalz FM, Quéguiner B, Bowler C (2018) Competition between silicifiers and non-silicifiers in the past and present ocean and its evolutionary impacts. Front Mar Sci 5:article 22

    Google Scholar 

  • Henrickson K, Stipp SLS (2009) Controlling biomineralisation: the effect of solution composition on coccolith polysaccharide functioning. Crystal Growth Design 9:2088–2097

    Google Scholar 

  • Henrickson K, Stipp SLS, Young JR, Marsh ME (2004) Biological control of calcite crystallization: AFM investigation of coccolith polysaccharide function. Am Mineral 89:1709–1716

    Google Scholar 

  • Heyduk K (2022) Evolution of crassulacean acid metabolism in relation to the environment: past, present and future. Plant Physiol 190:19–30

    PubMed  PubMed Central  Google Scholar 

  • Hoefs J (1969) Natural calcium oxalate with heavy carbon. Nature 223:396

    Google Scholar 

  • Hoffmann BA, Bernasconi SM (1998) Review of occurrences and carbon isotope geochemistry of oxalate minerals: implications for the origin and fate of oxalate in diagenetic and hydrothermal fluids. Chem Geol 149:127–146

    Google Scholar 

  • Horner HT, Wagner BT (1980) The association of druse crystals with the developing stomium of Capsicum annuum (Solanaceae) anthers. Am J Bot 67:531–541

    Google Scholar 

  • Horner HT, Wagner PT (1992) Association of four different calcium crystals in the anther connective tissue and hypodermal stomium of Capsicum annuum (Solanaceae) during microsporogenesis. Am J Bot 79:531–541

    Google Scholar 

  • Hudgins JW, Krekling T, Franceschi VR (2003) Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defence mechanism? New Phytol 159:677–670

    PubMed  Google Scholar 

  • Huguet A, Bernard S, Elkhatib R, Goke MI, Wiesenberg LB, Devenne S (2021) Multiple stages of plant root calcification deciphered by chemical and micromorphological analyses. Geobiology 19:75–86

    PubMed  Google Scholar 

  • Hynes A (1982) Stability of the oceanic tectosphere – a model of early Proterozoic intercratonic ontogeny. Earth Planet Sci Lett 61:333–345

    Google Scholar 

  • Iha C, Dougan KE, Varela JA, Avila V, Jackson CJ, Bogaert KA, Chen Y, Judd LM, Wick R, Holt KE, Pasella NM, Ricci F, Repetti SI, Medina M, Marcelino WR, Chan CX, Verbruggen H (2021) Genomic adaptations to an endolithic lifestyle in the coral-associated algae Ostreobium. Curr Biol 31:1393–1402

    PubMed  Google Scholar 

  • Ikka T, Ogawa T, Li D, Hiradate S, Morita A (2013) Effect of aluminium on metabolism of organic acids and chemical form of aluminium in Eucalyptus camaldulensis Dehnh. Phytochemistry 94:142–147

    PubMed  Google Scholar 

  • Iluz D, Fermani S, Ramot M, Reggi M, Cavoseli E, Prada F, Dubonsku Z, Goffredo S, Falina G (2017) Calcifying response and recovery potential of the brown alga Padina pavonica under ocean acidification. ACS Earth Space Sci 6:316–323

    Google Scholar 

  • Islam MN, Kawasaki M (2015) Evolution of calcium regulating roles of guttation and calcium oxalate crystals in leaf blades of hydroponically grown Eddo. Plant Prod Sci 18:11–21

    Google Scholar 

  • Jaillard B (1992) Calcification des cellules corticoles des raciness en milieu calcaire. Bull Soc Botan Francais 139, Actualite Botanique (1):41–46

    Google Scholar 

  • Jantschke A, Pinkas I, Schertel A, Addadi L, Weiner S (2020) Biomineralisation pathways in calcifying dinoflagellates: Uptake, storage in MgCaP-rich bodies and formation of the shell. Acta Biomater 102:427–439

    PubMed  Google Scholar 

  • Joy KW (1964) Accumulation of oxalate in the tissue of sugar-beet, and the effect of nitrogen supply. Ann Bot 28:689–701

    Google Scholar 

  • Kadan Y, Tollervey P, Varsano N, Mahadim J, Gal A (2021) Intracellular nanoscale architecture as a master regulator of calcium carbonate crystallization in marine microalgae. Proc Natl Acad Sci U S A 118:e205670118

    Google Scholar 

  • Kah LC, Riding R (2007) Mesoproterozoic carbon dioxide levels inferred from calcified cyanobacteria. Geology 35:799–802

    Google Scholar 

  • Karabourniotis G, Horner HT, Breista P, Nikopoulos D, Liakopoulos G (2020) New insights on the function of carbon-calcium-inclusions in plants. New Phytol 228:845–854

    PubMed  Google Scholar 

  • Karabourniotis G, Liakopoulos D, Breisto P, Nikopoulos D (2021) The optical properties of leaf structural elements and their contribution to photosynthetic performance and photoprotection. MDPI Plants 10:1455

    Google Scholar 

  • Kawahata O, Kamaura M, Shiraiwa Y (2013) Changes in alkaline band formation and calcification of corticated Chara globularis. SpringerPlus 2:95

    Google Scholar 

  • Kellermeier M, Meleno-Garcia E, Glanb F, Klein R, Drechler M, Rachel R, Garcia-Ruiz JM, Kuntz W (2010) Stabilisation of amorphous calcium carbonate in organic silica-rich environments. J Am Chem Soc 132:17859–17866

    PubMed  Google Scholar 

  • Kevin MJ, Hall WT, McLaughlin JJA, Zahl PA (1969) Symbiodinium microadriaticum Freudenthal, a revised taxonomic description, ultrastructure. J Phycol 5:341–350

    PubMed  Google Scholar 

  • Kidd PS, Llugang M, Poschnrieder C, Guosé B, Barceló J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352

    PubMed  Google Scholar 

  • Korth KL, Doege SJ, Park S-H, Goggin FL, Wang Q, Gomez K, Liu G, Jia L, Makata PA (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195

    PubMed  PubMed Central  Google Scholar 

  • Kraft GT, Saunders GW, Abbott IA, Haroun FJ (2004) A uniquely calcified brown alga from Hawaii: Newhousia imbricata gen. et sp nov. (Dictyotales, Phaeophyceae). J Phycol 40:383–394

    Google Scholar 

  • Kranz SA, Wolf-Gladrow D, Nehrke G, Langer G, Rost B (2010) Calcium carbonate precipitation induced by the marine cyanobacterium Trichodesmium. Limnol Oceanogr 15:2563–2569

    Google Scholar 

  • Kuo-Huang L-L, Sheue C-R, Yang Y-P, Chiang S-HT (1994) Calcium oxalate crystals in some aquatic angiosperms of Taiwan. Bot Bull Acad Sin 34:179–188

    Google Scholar 

  • Kuo-Huang L-L, Ku MSB, Franceschi VR (2007) Correlations between calcium oxalate crystals and photosynthetic activities in palisade cells of shade-adapted Peperomia glabella. Bot Stud 48:155–164

    Google Scholar 

  • Lajeunesse TC (2017) Validation and description of Symbiodinium microadriaticum, the type species of Symbiodinium (Dinophyta). J Phycol 53:1109–1114

    PubMed  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant and Soil 321:83–115

    Google Scholar 

  • Langer G, Taylor AR, Walker CE, Meyer EM, Ben Joseph O, Gal A, Harper GH, Probert I, Brownlee C, Wheeler GL (2021) The role of silicon in the development of crystal shapes in coccolithophores. New Phytol 231:1845–1857

    PubMed  Google Scholar 

  • Larbi A, Morales F, Albadia A, Albadia J (2010) Changes in iron and organic acid concentration in xylem sap and apoplastic fluids of iron-deficient Beta vulgaris plants in response to iron resupply. J Plant Physiol 167:255–260

    PubMed  Google Scholar 

  • Leganés F, Forchhammer K, Fernández-Piñas F (2009) Role of calcium in acclimation of the cyanobacterium PCC 7942 to nitrogen starvation. Microbiology 155:25–34

    PubMed  Google Scholar 

  • Lev-Yadun S, Halpern M (2008) External and internal spines in plants insert pathogenic microorganisms into herbivores for defense. In: van Dijk T (ed) Microbial ecology research trends Nova Science Publisher, Inc., pp 155–168

    Google Scholar 

  • Li J, Oliver IM, Cam N, Boudier T, Blondeau M, Lerey E, Cosmidis J, Skouri-Paret F, Guigner J-M, Férard C, Poinsot M, Moreira D, Lopez-Garcia P, Cassier-Cauvot C, Chauvot F, Benzerara K (2016) Biomineralization patterns of intracellular carbonate genesis in cyanobacteria: molecular hypotheses. Minerals 6. article 10

    Google Scholar 

  • Littler MM, Kauker BJ (1984) Heterotrichy and survival strategies in the red alga Corallina officinalis. Bot Mar 27:37–47

    Google Scholar 

  • Littler MM, Littler DS (2013) The nature of crustose coralline red alga and their interaction on reefs. Smithsonian Contrib Mar Sci 39:199–212

    Google Scholar 

  • Liu J, Bi B, Tian G, Li Z, Wang W, Ma F, Shi H, Liu W (2022) Crystal idioblasts are involved in the anther dehiscence of Nicotiana tabacum. Physiol Plant 174:e13753

    PubMed  Google Scholar 

  • Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24

    PubMed  PubMed Central  Google Scholar 

  • Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652

    PubMed  PubMed Central  Google Scholar 

  • Ma Z, Miyasaki SC (1998) Oxalate exudation by Taro in response to Al. Plant Physiol 118:861–865

    PubMed  PubMed Central  Google Scholar 

  • Malekhosseini M, Ensikat H-J, McCoy VE, Wappler T, Weigend M, Kunzmann L, Rust J (2022) Traces of calcium oxalate biomineralization in fossil leaves from the late Oligocene maar deposits from Germany. Sci Rep 12:15959

    PubMed  PubMed Central  Google Scholar 

  • Martignier A, Pacton M, Filella M, Jaquet JM, Barja F, Pollok K, Langenhorst F, Lavigne S, Gucagliardo P, Kilburn MR, Thomas C, Martini R, Ariztegui D (2017) Intracellular amorphous carbonates uncover a new biomineralization process in eukaryotes. Geobiology 15:240–253

    PubMed  Google Scholar 

  • Martignier A, Filella H, Pollak K, Melkonian M, Bensimon M, Barja F, Langenhent F, Jaquet J-M, Aristegui D (2018) Marine and freshwater micro pearls: biomineralization producing strontium-rich amorphous calcium carbonate inclusion is widespread in the genus Tetraselmis (Chlorophyta). Bigeosciences 15:6591–6605

    Google Scholar 

  • Martinelango PK, Dasgulta PK, Al-Horr RS (2007) Atmospheric production of oxalic acid/oxalate and nitric acid/nitrate in the Tampa Bay airshed: parallel pathways. Atmos Environ 41:4258–4269

    Google Scholar 

  • Martone PT (2006) Size, strength and allometry of joints in the articulated coralline Calliarthron. J Exp Biol 209:1678–1689

    PubMed  Google Scholar 

  • Martone PT, Kost L, Boller M (2012) Drag reduction in wave-swept macroalgae: alternative strategies and new predictions. Am J Bot 99:806–815

    PubMed  Google Scholar 

  • Mayers KMJ, Poulton AJ, Bidle K, Thaumatrakoln K, Schieler B, Gienig SLC, Wells SR, Tarran GA, Mayor D, Johnson M, Riebesell U, Larsen A, Vardi A, Hauvey L (2020) The possession of coccoliths fails to deter microzooplankton grazers. Front Mar Sci 7:569996

    Google Scholar 

  • McConnico LA, Foster MS, Dl S, Riosmena-Rodríguez R (2014) Population biology of a long-lived rhodolith: the consequences of becoming old and large. Mar Ecol Prog Ser 504:109–118

    Google Scholar 

  • Mehta N, Bougouve J, Kocar BD, Duprat E, Benzerara K (2022) Cyanobacteria accumulate radon (226Ra) within amorphous calcium carbonate inclusions. ACT EST Water 2:616–623

    Google Scholar 

  • Meier KJS, Young JR, Kirsch M, Reist-Burkhardt S (2007) Evolution of different life-cycle strategies in oceanic calcareous dinoflagellates. Eur J Phycol 42:81–89

    Google Scholar 

  • Miedema H, Prins HBA (1992) Coupling of proton fluxes in the polar leaves of Potamogeton lucens L. J Exp Bot 43:907–914

    Google Scholar 

  • Mitchell P (2011) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation 1996. Biochim Biophys Acta 1807:1507–1528

    PubMed  Google Scholar 

  • Mock T (2021) Silicon drives the evolution of complex crystal morphology in calcifying algae. New Phytol 251:1663–1666

    Google Scholar 

  • Molano-Flores B (2001) Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot 88:387–391

    Google Scholar 

  • Mondecai GJ, Verret F, Highfield A, Schroeder DC (2017) Schröedinger’s Cheshire Cat: are haploid Emiliania huxleyi cells resistant to viral infection or not. Viruses MDPI 9:51

    Google Scholar 

  • Monje PV, Baran EJ (2002) Characterization of calcium oxalates generated as biominerals in cacti. Plant Physiol 128:707–713

    PubMed  PubMed Central  Google Scholar 

  • Monje PV, Baran EJ (2010) Characterization of calcium oxalate biominerals in some (non-Cactaceae) succulent plant species. Zeits Naturforsch 65c:429–432

    Google Scholar 

  • Monteiro FM, Bach LT, Brownlee C, Bown P, Rickaby REM, Poulton AJ, Tyrell T, Beaufort L, Ditkeiwicz S, Gibb S, Gutwska MA, Lee R, Riebesell U, Young J, Ridgwell A (2016) Why marine phytoplankton calcify. Sci Adv 2:e1501822

    PubMed  PubMed Central  Google Scholar 

  • Moreira D, Tavera R, Benzerara K, Skori-Panet F, Couradeau E, Gérard E, Fonta CL, Nvelo E, Zuvarov Y, López-Garcia P (2017) Description of Gloeomargarita lithophora gen. nov., sp. nov., a thylakoid-bearing basal cyanobacterium with intracellular carbonates and proposal for Gloeomargaritales ord. nov. Int J Syst Evol Microbiol 67:653–658

    PubMed  Google Scholar 

  • Morita A, Tuji M (2002) Nitrate and oxalate contents of tea plants (Camellia sinensis L.) with special reference to the types of green tea and effects of shading. Soil Sci Plant Nutr 48:547–552

    Google Scholar 

  • Morita A, Suzuki R, Yokota M (2004) Effect of ammonium application on the oxalate content of the tea plant (Camellia sinensis L.). Soil Sci Plant Nutr 50:763–769

    Google Scholar 

  • Muller-Parker G, Lee KW, Cook CB (1996) Changes in the ultrastructure of symbiotic zooxanthellae (Symbiodinium sp, Dinophyceae) in fed and starved sea anemones maintained under high and low light. J Phycol 32:987–994

    Google Scholar 

  • Neustupa J, Nemcova Y (2022) Geometric morphometrics shows a close relationship between the shape features, position on thalli, and CaCO3 content of segments in Halimeda tuna (Bryopsidales, Ulvophyceae). Hydrobiologia 849:669–678

    Google Scholar 

  • O’Connell AM, Makzuk N, Gailitis V (1993) Occurrence of calcium oxalate in Karri (Eucalyptus diversicolor F. Muell. ) forest ecosystem of south western Australia. Oecologia 56:239–244

    Google Scholar 

  • Oka K, Kagawa A (1996) Effect of nitrogen nutrients on the oxalate content of Spinacia oleracea. J Japan Hort Soc 65:327–332

    Google Scholar 

  • Okazaki M, Pentecost A, Tanaka Y, Miyata M (1986) A study of calcium carbonate deposition in the genus Padina (Phaeophyceae, Dictyotales). Br Phycol J 21:217–224

    Google Scholar 

  • Okazaki M, Stoguchi H, Hisanaga E (1991) Inorganic composition of cystoliths isolated from leaves of higher plants. In: Suga S, Nakahara H (eds) Mechanisms and phylogeny of mineralisation in biological systems. Springer, Tokyo, pp 173–177

    Google Scholar 

  • Oscarsson V, Savage GP (2007) Composition and availability of soluble and insoluble oxalate in raw and cooked taro (Colocasia esculenta var Schott) leaves. Food Chem 101:559–562

    Google Scholar 

  • Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29:379–414

    Google Scholar 

  • Paasche E (1998) Roles of nitrogen and phosphorus in coccolith formation in Emiliania huxleyi (Prymnesiophyceae). Eur J Phycol 33:33–42

    Google Scholar 

  • Paasche E (1999) Reduced coccolith calcite production under light-limiting growth: a comparative study of three clones of Emiliania huxleyi (Prymnesiophyceae). Phycologia 38:508–516

    Google Scholar 

  • Paiva EAS (2019) Are calcium oxalate crystals a dynamic calcium store in plants? New Phytol 223:1707–1711

    PubMed  Google Scholar 

  • Paiva EAS (2021) Do calcium oxalate crystals protect against herbivory? Sci Nat 108:24

    Google Scholar 

  • Pantazidou A, Louvrou I, Economou-Amilh A (2006) Endolithic shell-boring cyanobacteria and chlorophytes from the saline lagoon Ahivadolimni on Milos Island, Greece. Eur J Phycol 41:189–200

    Google Scholar 

  • Park IS, Doege SJ, Nakata PA, Korth KL (2009) Medicago trunculata-derived calcium oxalate crystals have a negative impact on chewing insect performance via their physical properties. Entomol Exp Appl 151:208–215

    Google Scholar 

  • Peña V, Viera C, Braga JC, Aguirre J, Rösler A, Baele G, Clerk OD, Le Gall L (2020) Radiation of the coralline red algae (Corallinophycideae, Rhodophyta) crown group as inferred from a multilocus time-calibrated phylogeny. Mol Phylogenet Evol 150:106843

    Google Scholar 

  • Perry CT, Beavington-Penney SJ (2005) Epiphytic calcium carbonate production and facies development within sub-tropical seagrass beds, Inhaca Island, Mozambique. Sediment Geol 174:161–176

    Google Scholar 

  • Pierantoni M, Tenne R, Brumfeld V, Kiss V, Oron D, Addadi L, Weiner S (2017) Plants and light manipulation: the integrated mineral system in okra leaves. Adv Sci 4:1600416

    Google Scholar 

  • Pierantoni M, Tenne R, Raphael B, Brumfeld V, von Casteven A, Kupzik K, Oron D, Addadi L, Weiner S (2018) Mineral deposits in Ficus leaves: morphologies and locations in relation to function. Plant Physiol 176:1751–1763

    PubMed  Google Scholar 

  • Pierantoni M, Paudel I, Raphael B, Tenne R, Brumfeld V, Slomka S, Oron D, Addadi L, Weiner S, Klein Y (2020) Cystoliths in Ficus leaves: increasing carbon fixation in saturating light by light scattering off a mineral substrate. BioRχiv. https://doi.org/10.1101/2020/04.08.030999

  • Pivata N, Ballotari M (2021) Chlamydomonas reinhardtii cellular compartments and their contribution to intracellular calcium signalling. J Bot 72:5312–5355

    Google Scholar 

  • Prasad PVD, Chowdary YBK (1982) Nature and composition of the mineral deposition in the freshwater alga Gloeotaenium loitlesbergarianum Hansgirg (Chlorophyta, Chlorococcales). Phycologia 21:323–326

    Google Scholar 

  • Pratt BR (1982) Stromatolite decline: a reconsideration. Geology 10:512–515

    Google Scholar 

  • Prince JS (2012) Raphides in the uncalcified siphonous green seaweed Codium minus (Schmidt) P.C Silva. J Mar Biol 2012:382498

    Google Scholar 

  • Prins HBA, DeGuia MB (1986) Carbon sources of the water soldier, Stratiotes aloides L. Aquat Bot 26:225–234

    Google Scholar 

  • Pueschel CM (1995) Calcium oxalate crystals in the red alga Antithamnion kylinii (Ceramiales): cytoplasmic and limited to indeterminate axes. Protoplasma 189:73–80

    Google Scholar 

  • Pueschel CM (2001) Calcium oxalate crystals in the green alga Spirogyra hatillensis (Zygnematales, Chlorophyta). Int J Plant Sci 162:1337–1345

    Google Scholar 

  • Pueschel CM (2002) Calcium oxalate crystals in the green alga Spirogyra sp. (Zygnematales, Chlorophyta). J Phycol 36:55–56

    Google Scholar 

  • Pueschel CM (2019) Calcium oxalate mineralisation in algae. Phycologia 58:331–350

    Google Scholar 

  • Pueschel CM, West JA (2002) Cytoplasmic streaming of calcium oxalate crystals in Callipsygma wilsonis (Bryopsidales, Chlorophyta). Phycol Res 55:278–285

    Google Scholar 

  • Pueschel CM, West JA (2007a) Cytoplasmic streaming of calcium oxalate crystals in Callipsygma wilsonis (Bryopsidales, Chlorophyta). Phycol Res 55:278–285

    Google Scholar 

  • Pueschel CM, West JA (2007b) Calcium oxalate crystals in the marine red alga Spyridia filamentosa (Ceramiales, Rhodophyta). Phycologia 46:565–571

    Google Scholar 

  • Pueschel CM, West JA (2011) Cellular location of calcium oxalate crystals in Chaetomorpha coliformis (Cladophorales, Chlorophyta): evidence of vacuolar differentiation. Phycologia 50:430–435

    Google Scholar 

  • Quade BN, Parker MD, Hoepflinger MC, Phipps S, Bisson MA, Foissner I, Beilby MJ (2022) The molecular identity of the characean OH− transporter: a candidate related to the SLC4 family of animal pH regulation. Protoplasma 259:615–626

    PubMed  Google Scholar 

  • Quinitero-Torres R, Aragón JL, Torres M, Estrado M, Cros L (2006) Strong far-field coherent scattering by holococcolithophores. Phys Rev E 74:032901

    Google Scholar 

  • Radtke G, Gektidis M, Golubic S, Hofman K, Kiene WE, Le Combion-Alsunard T (1997) The identity of the endolithic alga Ostreobium brabantium Weber van Bosse is recognised as carbonate-penetrating rhizoids of Acetabularia (Dasycladales). Cour Forsch-Inst Senckenburg 201:341–357

    Google Scholar 

  • Rae BD, Long BM, Badger MR, Price GD (2013) Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in Cyanobacteria and some Protobacteria. Microbiol Mol Biol Rev 77:357–379

    PubMed  PubMed Central  Google Scholar 

  • Rahman MM, Ishi Y, Niimi M, Kawamura O (2010a) Effect of application form of nitrogen on oxalate accumulation and mineral uptake by napiergrass (Pennisetum purpureum). Grassland Sci 56:141–144

    Google Scholar 

  • Rahman MM, Ishii Y, Niimi M, Kawamura O (2010b) Interactive effects of nitrogen and potassium fertilization on oxalate content in napiergrass (Pennisetum purpureum). Asian-Austral J Animal Sci 23:719–723

    Google Scholar 

  • Ramírez-Reinet E, Garcia-Pichel F (2012) Prevalence of Ca2+-ATPase-mediated carbonate dissolution among cyanobacterial euendoliths. Appl Environ Microbiol 78:7–13

    Google Scholar 

  • Ramos GJP, de Oliveira IB, de Nascimento Moira CW (2021) On the occurrence of the mineral deposition in the freshwater alga Gloeotaenium (Oocystaceae, Trebouxiophyceae). Rodriguèsiana 72:01372019

    Google Scholar 

  • Ratcliffe S, Meyer EM, Walker CEE, Knight M, McNair NM, Matson PG, Iglesias-Rodriguez D, Brzezinski M, Langer G, Sadelar A, Greaves M, Brownlee C, Currow P, Taylor AR, Wheeler GL (2022) Characterization of the molecular mechanisms of silicon uptake in coccolithophores. Environ Microbiol. https://doi.org/10.1111/i462-2200.16280

  • Raven JA (1977) H+ and Ca2+ in phloem and symplasm: relation of relative immobility of the ions to the cytoplasmic nature of the transport paths. New Phytol 79:465–480

    Google Scholar 

  • Raven JA (1981) Nutritional strategies of submerged benthic plants the acquisition of C, N and P by rhizophytes and haptophytes. New Phytol 88:1–30

    Google Scholar 

  • Raven JA (1984) Energetics and transport in aquatic plants. A.R. Liss, New York, pp ix + 587

    Google Scholar 

  • Raven JA (1986) Biochemical disposal of excess H+ in growing plants? New Phytol 104:175–206

    Google Scholar 

  • Raven JA (1996) Into the voids: The distribution, function, development and maintenance of gas spaces in plants. Ann Bot 78:137–142

    Google Scholar 

  • Raven JA (2017) The possible roles of algae in restricting the increase in atmospheric CO2 and global temperature. Eur J Phycol 58:506–522. https://doi.org/10.10180/09670262.1362593

    Article  Google Scholar 

  • Raven JA (2018) Blue carbon: past, present and future, with emphasis on macroalgae. Biol Lett 14:20180336

    PubMed  PubMed Central  Google Scholar 

  • Raven JA, Andrews M (2023) Photon costs of shoot and root NO3−, and root NH4+. Assimilation in terrestrial vascular plants considering associated pH regulation, osmotic and ontogenetic effects. Photosynth Res 155:127–137. https://doi.org/10.1007/s1112o-022-00975-y

  • Raven JA, Edwards DE (2000) Roots: evolutionary origin and biogeochemical significance. J Exp Bot 52:381–401

    Google Scholar 

  • Raven JA, Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of isotopes of carbon in plants. New Phytol 116:505–529

    PubMed  Google Scholar 

  • Raven JA, Giordano M (2009) Biomineralisation by photosynthetic organisms: evidence of coevolution of the organisms and their environment. Geobiology 7:140–154

    PubMed  Google Scholar 

  • Raven JA, Smith FA (1976) Nitrogen assimilation and transport in vascular plants in relation to intracellular pH regulation. New Phytol 76:415–431

    Google Scholar 

  • Raven JA, Spicer RA (1996) The evolution of crassulacean acid metabolism. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism, ecological studies volum 14. Springer, Berlin, pp 360–385

    Google Scholar 

  • Raven JA, Waite A (2004) The evolution of silicification in diatoms: inescapable sinking and sinking to escape? New Phytol 163:45–61

    Google Scholar 

  • Raven JA, Griffiths H, Glidewell SM, Preston T (1982) The mechanism of oxalate biosynthesis in higher plants: investigations with the stable isotopes 18O and 13C. Proc R Soc B 216:87–191

    Google Scholar 

  • Resentini F, Ruberti C, Grenzi M, Bonza MC, Costa A (2021) The signatures of organellar calcium. Plant Physiol 187:1985–2004

    PubMed  PubMed Central  Google Scholar 

  • Richardson PT, Baker DA, Ho LC (1982) The chemical composition of cucurbit vascular sap. J Exp Bot 33:1239–1242

    Google Scholar 

  • Riding R (2000) Microbial carbonates: the geological record of calcified cyanobacterial-algal mats and biofilms. Sedimentology 47:179–214

    Google Scholar 

  • Riding R (2006) Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4:299–316

    Google Scholar 

  • Riding JB, Fensome RA, Soyer-Gobillard M-O, Medlin LK (2023) A review of the dinoflagellates and evolution from fossils to modern. J Mar Sci Eng 11:1

    Google Scholar 

  • Rishworth GM, Perisinotto R, Bird MS (2016) Coexistence of living stromatolites and infaunal metazoans. Oecologia 182:539–545

    PubMed  Google Scholar 

  • Rishworth GM, Perisinotto R, Bird MS (2017a) Patterns and drivers of benthic macrofaunal communities dwelling within extant peritidal stromatolites. Lmnol Oceangr 62:2227–2242

    Google Scholar 

  • Rishworth GM, Perisinotto R, Bird MS, Strydom NA, Per N, Miranda NAF, Raw JL (2017b) Non-reliance of metazoans on stromatolite-forming microbial mats as a food resource. Sci Rep 7:426114

    Google Scholar 

  • Rivera ER, Smith BN (1979) Crystal morphology and 13Carbon/12Carbon composition of solid oxalate in cacti. Plant Physiol 6:966–970

    Google Scholar 

  • Rokitta JD, John U, Rost B (2012) Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi. PloS One 7:52212

    Google Scholar 

  • Rott E, Holzinger A, Gesierich D, Kofler W, Cardeno D (2010) Cell morphology, ultrastructure, and calcification patterns in Oocardium stratum, a peculiar lotic desmid. Protoplasma 243:49–50

    Google Scholar 

  • Ruiz N, Ward M, Saltz D (2002a) Calcium oxalate crystals in leaves of Pancratium sickenbergeri : constitutive or induced defence. Funct Ecol 16:99–105

    Google Scholar 

  • Ruiz N, Ward M, Saltz D (2002b) Response of Pancratium sickenbergeri to simulated bulb herbivory: combining deference and tolerance strategies. J Ecol 90:4720479

    Google Scholar 

  • Sanchez-Báracaldo P (2015) Origin of marine planktonic cyanobacteria. Sci Rep 5:17418

    PubMed  PubMed Central  Google Scholar 

  • Sand-Jensen K, Jensen RS, Gomes M, Kristensen R, Martinson KT, Kragh T, Spohr LB, Borum J (2018) Photosynthesis and calcification of charophytes. Aquat Bot 149:46–51

    Google Scholar 

  • Segovia-Campos I, Martignier A, Filella M, Jacquet J-M, Arisztgui D (2022) Micropearls and intracellular inclusions of amorphous calcium carbonate: an unsuspected biomineralization capacity shared by diverse microorganisms. Environ Microbiol 24:537–550

    PubMed  Google Scholar 

  • Shervais JW, Taylor LA, Lugmair GW, Clayton RN, Mayeda TK, Korolov RL (1988) Early Proterozoic ocean crust and the evolution of subcontinental mantle: eclogites and related rocks from South Africa. Geol Soc Am Bull 100:411–423

    Google Scholar 

  • Shewin S, Gowns DA (1995) Secondary growth and wood histology of Welwitschia. Bol J Linn Soc 118:107–121

    Google Scholar 

  • Sikes CS, Wilbur WM (1982) Functions of coccolithophore formation. Limnol Oceanogr 27:18–26

    Google Scholar 

  • Silver MW, Bruland KW (1981) Differential feeding and fecal pellet composition of salps and pteropods, and the possible role of deep water flora and olive-green ‘cells’. Mar Biol 62:263–273

    Google Scholar 

  • Simpson TS, Savage GP, Sherlock R, Canhanen LP (2009) Oxalate content of silver beet (Beta vulgaris var. cicla) at different stages and maturation and effects of cooking in different milk sources. J Agric Food Chem 57:10804–10808

    PubMed  Google Scholar 

  • Skeffington AW, Scheffel A (2018) Exploiting algal mineralization for nanotechnology: bringing coccoliths to the fore. Curr Opin Biotechnol 49:57–63

    PubMed  Google Scholar 

  • Smith AM, Sutherland JE, Kregting L, Farr TJ, Winter DJ (2012) Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny. Phytochemistry 81:97–108

    PubMed  Google Scholar 

  • Steneck RS (1983) Escalating herbivory and resulting adaptive traits in calcareous algal crusts. Palaeobiology 9:44–61

    Google Scholar 

  • Steneck RS (1985) Adaptations of crustose coralline algae to herbivory: patterns in space and time. In: Toomey DF, Nitaki MH (eds) Palaeoalgology, vol 15. Springer, Berlin, p. 15

    Google Scholar 

  • Steneck RS (1986) The ecology of coralline algal crusts: convergent patterns and adaptive strategies. Annu Rev Ecol Syst 17:273–303

    Google Scholar 

  • Steneck RS, Hacker SD, Dethier MN (1991) Mechanisms of competitive crustose coralline algae: an herbivore-mediated competitive reversal. Ecology 72:938–950

    Google Scholar 

  • Tao Q, Hou D, Yang X, Li T (2016) Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant and Soil 398:139–152

    Google Scholar 

  • Taylor KD (1968) In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate. J Mar Biol Assoc UK 48:349–366

    Google Scholar 

  • Taylor AM, Brownlee C, Wheeler GL (2017) Coccolithophore cell biology: chalking up progress. Ann Rev Mar Sci 9:283–310

    PubMed  Google Scholar 

  • Tebbon J, Matti CA, Siboni N, Tapoiolas GM, Negri AP, Schupp PJ, Kirtanama M, Hatta M, Steinberg PD, Harder T (2015) Chemical mediation of coral larvae settlement by crustose coralline algae. Sci Rep 5:10803

    Google Scholar 

  • Teichert S (2014) Hollow rhodoliths increase Svalbard’s shelf biodiversity. Sci Rep 4:6972

    PubMed  PubMed Central  Google Scholar 

  • Thompson JB, Schultze-Lam S, Berridge TJ, Des Marais DJ (1997) Whiting events biogenic origin due to the photosynthetic activity in cyanobacterial picoplankton. Limnol Oceanogr 42:133–141

    PubMed  Google Scholar 

  • Tian H, Jiang L, Liu E, Zhang J, Liu F, Peng X (2008) Dependence of nitrate-induced oxalate accumulation on nitrate reduction in rice leaves. Physiol Plant 133:180–189

    PubMed  Google Scholar 

  • Tooulakou G, Giannopoulos A, Nikopoulos D, Bresta P, Dotsika E, Orkoula MG, Kontoyannis CG, Fasseas C, Liakopoulos G, Klapa MI, Karabourniotis G (2016a) Alarm photosynthesis: calcium oxalate crystals as internal CO2 source in plants. Plant Physiol 171:2577–2585

    PubMed  PubMed Central  Google Scholar 

  • Tooulakou G, Giannopoulos A, Nikopoulos D, Bresta P, Dotsika E, Orkoula MG, Kontoyannis CG, Fasseas C, Liakopoulos G, Klapa MI, Karabourniotis G (2016b) Reevaluation of the plant “gemstones”: calcium oxalate crystals sustain photosynthesis under drought conditions. Plant Signal Behav 11:e1215793

    PubMed  PubMed Central  Google Scholar 

  • Tooulakou G, Nikopoulos D, Dotsika E, Orkoula MG, Kontoyannis CG, Liakopoulos G, Klapa MI, Karabourniotis G (2019) Changes in size and composition of pigweed (Amaranthus hybridus L.) calcium oxalate crystals under CO2 starvation conditions. Physiol Plant 166:862–872

    PubMed  Google Scholar 

  • Torrecilla I, Leganés F, Bonilla I, Fernández-Piñas F (2000) Use of recombinant aequorin to study calcium homeostasis and monitor calcium transient responses to heat and cold shock in cyanobacteria. Plant Physiol 123:161–176

    PubMed  PubMed Central  Google Scholar 

  • Troyo A, Jiménez-Duran K, van Tussenbroeck BI, Máaquez-Guzmán J, Wang GGR, Conena-Carrillo JI, Díaz-Pontanes DM (2021) Fruit development in the seagrass Thalassia testudinum. Possible relationship between structure, physiology and defence. Aquat Biol 174:103418

    Google Scholar 

  • Turekian VC, Macko SA, Keene WC (2003) Concentrations, isotope compositions, and source of size-resolved organic carbon and oxalate in near-surface marine air at Bermuda during spring. J Geophys Res 108:article D14. https://doi.org/10.1029/2002JD002053

    Article  Google Scholar 

  • Tyrell T, Holligan PM, Mobley CD (1999) Optical impacts of ocean coccolithophore blooms. J Geophys Res 104(C2):3223–3241

    Google Scholar 

  • Vale NFL, Braga JC, Bastos AC, Moraes FC, Kavez CS, Bahia RG, Leão LA, Pereira RC, Amado-Filho GM, Salgado LT (2022) Structure and composition of rhodolith beds from Sergipe-Alagoas GM, Sakgado LT (2022) Structure and composition of rhodolith beds from Sergipe-Alagoas Basin (NE Brazil, Southwestern Atlantic). Diversity MDPI 14:282

    Google Scholar 

  • Van de Waal DB, John U, Ziveri P, Reichart G-J, Hoins M, Sluijs A, Rost B (2013) Ocean acidification reduces growth and calcification in a marine dinoflagellate. PloS One 8:e65987

    PubMed  PubMed Central  Google Scholar 

  • van Ginkel LC, Bowes G, Reiskind JB, Prins HBA (2001) A CO2-flux mechanism operating via pH polarity in Hydrilla verticillata leaves with C3 and C4 photosynthesis. Photosynth Res 68:81–88

    PubMed  Google Scholar 

  • Vogelmann TC (1993) Plant tissue optics. Annu Rev Plant Physiol Plant Mol Biol 44:231–251

    Google Scholar 

  • von Dassow P, Ogata H, Probert I, Wincker P, DaSilva C, Audic S, Claverie J-M, de Vargas P (2009) Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol 10:R114

    Google Scholar 

  • von Dassow P, van den Engh G, Iglesias-Rodriguez D, Gittins JB (2012) Calcification state of coccolithophores can be assessed by light scattering depolarisation experiments with flow cytometry. J Plankton Res 34:1011–1027

    Google Scholar 

  • Wakefield TS, Farmer MA, Kempf SC (2000) Revised description of the fine structure in situ ‘zooxanthellae’ genus Symbiodinium. Biol Bull 199:76–84

    PubMed  Google Scholar 

  • Walker NA, Smith FA, Cather IR (1980) Bicarbonate assimilation by freshwater by freshwater charophytes and higher plants. I. Membrane transport of bicarbonate ions is not proven. J Membr Biol 57:51–58

    Google Scholar 

  • Walker CE, Taylor AR, Langer G, Durak GM, Heath S, Probert I, Tyrell T, Brownlee C, Wheeler GL (2018) The requirement for calcification differs between ecologically important coccolithophore species. New Phytol 220:147–162

    PubMed  PubMed Central  Google Scholar 

  • Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of the desert lily. J Chem Ecol 23:333–346

    Google Scholar 

  • Wendler JE, Bown P (2012) Exceptionally well-preserved Cretaceous microfossils reveal new biomineralisation styles. Nat Commun 4:2052

    Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    PubMed  PubMed Central  Google Scholar 

  • Whiteman R, Wallis S, Aston P (2018) Leaf margin organisation and the existence of vaterite-producing hydathodes in the alpine plant Saxifraga scardica. Flora 241:27–34

    Google Scholar 

  • Williams S, Halfar J, Zack T, Hetzinger S, Bladher M, Juul-Pedersen T (2018) Comparison of climate signals obtained from encrusting and free-living rhodolith coralline algae. Chem Geol 476:418–428

    Google Scholar 

  • Winter K, Smith JAC (2022) CAM photosynthesis: the acid test. New Phytol 233:19–30

    Google Scholar 

  • Wu J, Ceilfus V-M, Pitann B, Mühling K-H (2016) Silicon-enhanced oxalate exudation contributes to alleviation of cadmium toxicity in wheat. Environ Exp Bot 131:10–18

    Google Scholar 

  • Wyness AJ, Roush D, McQuaid CD (2022) Global distribution and diversity of marine endolithic cyanobacteria. J Phycol 58:746–759

    PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Tholen D, Zhu X-G (2016) The influence of leaf anatomy on the internal light environment and photosynthetic electron transport rate: exploration with a new leaf ray tracing model. J Exp Bot 67:6021–6035

    PubMed  PubMed Central  Google Scholar 

  • Yang JL, Zheng SJ, He YF, Matsumoto H (2005) Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot 56:1197–1203

    PubMed  Google Scholar 

  • Zhang Y, Lin Y, Zhang Y, Zheng SJ, Du S (2005) Effects of nitrogen levels and nitrate/ammonium ratios on oxalate concentrations of different forms in edible parts of spinach. J Plant Nutr 28:2011–2025

    Google Scholar 

  • Zhang C, Yu X, Ayre BG, Turgeon R (2012) The origin and composition of cucurbit ‘phloem’ exudate. Plant Physiol 158:1873–1882

    PubMed  PubMed Central  Google Scholar 

  • Zinssmeister C, Keupp H, Tischendorf G, Kaulbars F, Gottschling M (2013) Ultrastructure of calcareous dinophytes (Thoracosphaeraceae, Peridiniales) with a focus on vacuolar crystal-like particles. PloS One 8:54038

    Google Scholar 

  • Žuljević A, Katel S, Peña V, Despalatović M, Cvitković I, De Clerck O, Le Gall L, Falace A, Vita F, Braga JC, Antolić B (2016) First freshwater coralline alga and the role of local features in a major biome transition. Sci Rep 6:19642

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Discussions with Mitchell Andrews, Mary Beilby, Colin Brownlee, Dianne Edwards, Graham Farquhar, Mario Giordano*, Andrew Smith, Alison Taylor, Anya Waite, Glen Wheeler, and Philip White have been very useful.

*Deceased: 15-5-1964 – 29-12-2019.

The University of Dundee is a registered Scottish charity, No SC051096.

Author information

Authors and Affiliations

  1. Division of Plant Science, University of Dundee at the James Hutton Institute, Dundee, UK

    J. A. Raven

  2. Climate Change Cluster, University of Technology Sydney, Ultimo, NSW, Australia

    J. A. Raven

  3. School of Biological Sciences, University of Western Australia, Crawley, WA, Australia

    J. A. Raven

Authors
  1. J. A. Raven
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. A. Raven .

Editor information

Editors and Affiliations

  1. Department of Biology, Technical University of Darmstadt, Darmstadt, Germany

    Ulrich Lüttge

  2. Department of Molecular Biology and Biochemistry, University of Málaga, Málaga, Spain

    Francisco M. Cánovas

  3. Pollen Biotechnology of Crop Plants Group, Centro de Investigaciones Biologicas “Margarita Salas” (CIB) CSIC, Madrid, Madrid, Spain

    María-Carmen Risueño

  4. Plant Ecology, University of Göttingen, Göttingen, Germany

    Christoph Leuschner

  5. Chair for Forest Growth and Yield Science, School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Bayern, Germany

    Hans Pretzsch

Ethics declarations

Competing Interests

No competing interests are declared.

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Raven, J.A. (2023). Distribution and Functions of Calcium Mineral Deposits in Photosynthetic Organisms. In: Lüttge, U., Cánovas, F.M., Risueño, MC., Leuschner, C., Pretzsch, H. (eds) Progress in Botany Vol. 84. Progress in Botany, vol 84. Springer, Cham. https://doi.org/10.1007/124_2023_71

Download citation

Publish with us

Policies and ethics

Search

Navigation