Skip to main content

Circadian Regulation of Pineapple CAM Photosynthesis

  • Chapter
  • First Online:
Genetics and Genomics of Pineapple

Part of the book series: Plant Genetics and Genomics: Crops and Models ((PGG,volume 22))

Abstract

The altered carbon assimilation pathway of crassulacean acid metabolism (CAM) evolved as an adaptation to arid environments, and it confers 80% greater water use efficiency than the C3 pathway. Pineapple is the most economically valuable crop possessing CAM, and its wealth of genetic and genomic resources make it an excellent model for dissecting the molecular basis of this important pathway. Decades of physiology studies in pineapple identified the underlying biochemistry of CAM, but this work yielded little insight into the regulation and circadian control of CAM. High-resolution transcriptome surveys across the pineapple leaf gradient and throughout a diurnal time course were recently collected. This work uncovered new CAM-associated genes and suggested CAM evolved through neofunctionalization of existing gene copies and not through gene duplication events. CAM pathway genes are enriched with cis-regulatory elements associated with regulation by circadian clock genes. This includes novel clock-associated cis-regulatory elements in several stomatal movement genes, which may be related to nocturnal stomatal conductance in CAM plants. Together, these resources in pineapple provide a foundation for targeted engineering of CAM into C3 crop species.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
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

  • Antony E, Taybi T, Courbot M, Mugford ST, Smith JA, Borland AM (2008) Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). J Exp Bot 59:1895–1908

    Article  CAS  Google Scholar 

  • Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci U S A 109:10593–10598

    Article  CAS  Google Scholar 

  • Brautigam A, Schluter U, Eisenhut M, Gowik U (2017) On the evolutionary origin of CAM photosynthesis. Plant Physiol 174:473–477

    Article  Google Scholar 

  • Brilhaus D, Brautigam A, Mettler-Altmann T, Winter K, Weber AP (2016) Reversible burst of transcriptional changes during induction of crassulacean acid metabolism in talinum triangulare. Plant Physiol 170:102–122

    Article  CAS  Google Scholar 

  • Carnal NW, Black CC (1989) Soluble sugars as the carbohydrate reserve for CAM in pineapple leaves implications for the role of pyrophosphate: 6-phosphofructokinase in glycolysis. Plant Physiol 90:91–100

    Article  CAS  Google Scholar 

  • Cheffings CM, Pantoja O, Ashcroft FM, Smith JA (1997) Malate transport and vacuolar ion channels in CAM plants. J Exp Bot 48:623–631

    Article  CAS  Google Scholar 

  • Christopher JT, Holtum J (1996) Patterns of carbon partitioning in leaves of crassulacean acid metabolism species during deacidification. Plant Physiol 112:393–399

    Article  CAS  Google Scholar 

  • Costa JM, Monnet F, Jannaud D, Leonhardt N, Ksas B, Reiter IM, Pantin F, Genty B (2015) Open all night long: the dark side of stomatal control. Plant Physiol 167:289–294

    Article  CAS  Google Scholar 

  • Cushman JC, Agarie S, Albion RL, Elliot SM, Taybi T, Borland AM (2008) Isolation and characterization of mutants of common ice plant deficient in crassulacean acid metabolism. Plant Physiol 147:228–238

    Article  CAS  Google Scholar 

  • Dever LV, Boxall SF, Knerova J, Hartwell J (2015) Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiol 167:44–59

    Article  CAS  Google Scholar 

  • Dittrich P, Campbell WH, Black CC (1973) Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiol 52:357–361

    Article  CAS  Google Scholar 

  • Eom JS, Chen LQ, Sosso D, Julius BT, Lin IW, Qu XQ, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol 25:53–62

    Article  CAS  Google Scholar 

  • Grew N, Rawlins W (1682) The anatomy of plants with an idea of a philosophical history of plants, and several other lectures, read before the Royal Society. W. Rawlins, London

    Google Scholar 

  • Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K (2006) Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat Cell Biol 8:391–397

    Article  CAS  Google Scholar 

  • Hedrich R, Sauer N, Neuhaus HE (2015) Sugar transport across the plant vacuolar membrane: nature and regulation of carrier proteins. Curr Opin Plant Biol 25:63–70

    Article  CAS  Google Scholar 

  • Imes D, Mumm P, Bohm J, Al-Rasheid KA, Marten I, Geiger D, Hedrich R (2013) Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant J 74:372–382

    Article  CAS  Google Scholar 

  • Inada S, Ohgishi M, Mayama T, Okada K, Sakai T (2004) RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16:887–896

    Article  CAS  Google Scholar 

  • Kenyon WH, Severson RF, Black CC (1985) Maintenance carbon cycle in crassulacean acid metabolism plant leaves : source and compartmentation of carbon for nocturnal malate synthesis. Plant Physiol 77:183–189

    Article  CAS  Google Scholar 

  • Klein M, Perfus-Barbeoch L, Frelet A, Gaedeke N, Reinhardt D, Mueller-Roeber B, Martinoia E, Forestier C (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J 33:119–129

    Article  CAS  Google Scholar 

  • Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) From the cover: a role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci U S A 102:12270–12275

    Article  CAS  Google Scholar 

  • Matrosova A, Bogireddi H, Mateo-Penas A, Hashimoto-Sugimoto M, Iba K, Schroeder JI, Israelsson-Nordstrom M (2015) The HT1 protein kinase is essential for red light-induced stomatal opening and genetically interacts with OST1 in red light and CO2 -induced stomatal movement responses. New Phytol 208:1126–1137

    Article  CAS  Google Scholar 

  • Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

    Article  CAS  Google Scholar 

  • Ming R, VanBuren R, Wai CM, Tang H, Schatz MC, Bowers JE, Lyons E, Wang ML, Chen J, Biggers E, Zhang J, Huang L, Zhang L, Miao W, Ye Z, Miao C, Lin Z, Wang H, Zhou H, Yim WC, Priest HD, Zheng C, Woodhouse M, Edger PP, Guyot R, Guo HB, Guo H, Zheng G, Singh R, Sharma A, Min X, Zheng Y, Lee H, Gurtowski J, Sedlazeck FJ, Harkess A, McKain MR, Liao Z, Fang J, Liu J, Zhang X, Zhang Q, Hu W, Qin Y, Wang K, Chen LY, Shirley N, Lin YR, Liu LY, Hernandez AG, Wright CL, Bulone V, Tuskan GA, Heath K, Zee F, Moore PH, Sunkar R, Leebens-Mack JH, Mockler T, Bennetzen JL, Freeling M, Sankoff D, Paterson AH, Zhu X, Yang X, Smith JA, Cushman JC, Paull RE, Yu Q (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47:1435–1442

    Article  CAS  Google Scholar 

  • Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4:e327

    Article  Google Scholar 

  • Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2011) The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol 155:553–561

    Article  CAS  Google Scholar 

  • Suh SJ, Wang YF, Frelet A, Leonhardt N, Klein M, Forestier C, Mueller-Roeber B, Cho MH, Martinoia E, Schroeder JI (2007) The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J Biol Chem 282:1916–1924

    Article  CAS  Google Scholar 

  • Takemiya A, Shimazaki K (2016) Arabidopsis phot1 and phot2 phosphorylate BLUS1 kinase with different efficiencies in stomatal opening. J Plant Res 129:167–174

    Article  CAS  Google Scholar 

  • Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki K (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094

    Article  Google Scholar 

  • Tsutsumi T, Takemiya A, Harada A, Shimazaki K (2013) Disruption of ROOT PHOTOTROPISM2 gene does not affect phototropin-mediated stomatal opening. Plant Sci 201-202:93–97

    Article  CAS  Google Scholar 

  • Wai CM, VanBuren R, Zhang J, Huang L, Miao W, Edger PP, Yim WC, Priest HD, Meyers BC, Mockler T, Smith JAC, Cushman JC, Ming R (2017) Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. Plant J 92(1):19–30

    Article  CAS  Google Scholar 

  • Wang H, Ma LG, Li JM, Zhao HY, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294:154–158

    Article  CAS  Google Scholar 

  • Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH (2009) Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol 10:R68

    Article  Google Scholar 

  • Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2010) Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. J Biol Chem 285:1138–1146

    Article  CAS  Google Scholar 

  • Zeng W, Brutus A, Kremer JM, Withers JC, Gao X, Jones AD, He SY (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. Tomato DC3000. PLoS Pathog 7:e1002291

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Wai, C.M., VanBuren, R. (2018). Circadian Regulation of Pineapple CAM Photosynthesis. In: Ming, R. (eds) Genetics and Genomics of Pineapple. Plant Genetics and Genomics: Crops and Models, vol 22. Springer, Cham. https://doi.org/10.1007/978-3-030-00614-3_17

Download citation

Publish with us

Policies and ethics