Skip to main content
SpringerLink
Log in

Study on photosynthetic responses and chlorophyll fluorescence in Rhizophora mucronata seedlings under shade regimes

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The photosynthetic performance of mangrove Rhizophora mucronata seedlings grown under seasonally full light (HL), 50 % shade (ML), and 80 % shade (LL) conditions was characterized by gas exchange, and chlorophyll fluorescence. The carboxylation efficiency significantly affected the seasonal change of the photosynthetic capacity. Temperature and light might have synergic effect on the carboxylation efficiency. The photosynthetic rate (PN) of R. mucronata seedlings under shade regimes, however, could not be attributed to variability in chlorophyll, C i , ΦPSII, ETR or qP values but more to differences in carboxylation efficiency, g max, and E max. HL and ML plants had higher PN, g s and E than the LL ones. Nevertheless, LL leaves exhibited low photoinhibition susceptibility. The high non-photochemical quenching in HL leaves may show that applied light intensity probably exceeded the photosynthetic capability. The findings indicate that ML treatments provided the best condition to obtain such carbon fixation capacity.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

C i :

Intercellular CO2 concentration

E :

Transpiration rate

E max :

Maximum transpiration rate

ETR:

Electron transport rate

F v/F m :

Ratio of variable to maximum chlorophyll fluorescence

g max :

Maximum stomatal conductance

g s :

Stomatal conductance

PAR:

Photosynthetically active radiation

P max :

Maximum photosynthetic rate

P N :

Net photosynthetic rate

PSII:

Photosystem II

qN:

Non-photochemical quenching

qP:

Photochemical quenching

SPAD:

Soil plant analysis development

Vpdl:

Vapor pressure deficit between the leaf and air

ΦPSII:

Quantum yield of photosystem II

References

  • Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49. doi:10.1641/0006-3568(2004)054[0041:PSOOE]2.0.CO;2

    Article  Google Scholar 

  • Agata W, Hakoyama S, Kawamitsu Y (1985) Influence of light intensity, temperature and humidity on photosynthesis and transpiration of Sasa nipponica and Arundinaria pygmaea. Bot Mag Tokyo 98:125–135. doi:10.1007/BF02488792

    Article  Google Scholar 

  • Alam B, Nair DB, Jacob J (2005) Low temperature stress modifies the photochemical efficiency of a tropical tree species Hevea brasiliensis: effects of varying concentration of CO2 and photon flux density. Photosynthetica 43(2):247–252. doi:10.1007/s11099-005-0040-z

    Article  CAS  Google Scholar 

  • Alves PLCA, Magalhães ACN, Barja PR (2002) The phenomenon of photoinhibition of photosynthesis and its importance in reforestation. Bot Rev 68(2):193–208. doi:10.1663/0006-8101(2002)068[0193:TPOPOP]2.0.CO;2

    Article  Google Scholar 

  • Andrews TJ, Clough BF, Muller GJ (1984) Photosynthetic gas exchange and carbon isotope ratios in some mangrove species in North Queensland. In: Teas HJ (ed) Physiology and management of mangroves. (Tasks for vegetation science, vol 9). Junk, The Hague, pp 15–23

    Chapter  Google Scholar 

  • Bajkan S, Varkonyi Z, Lehoczki E (2012) Comparative study on energy partitioning in photosystem II of two Arabidopsis thaliana mutants with reduced non-photochemical quenching capacity. Acta Physiol Plant 34:1027–1034. doi:10.1007/s11738-011-0899-1

    Article  CAS  Google Scholar 

  • Ball MC (1986) Photosynthesis in mangrove. Wetlands 6(1):12–22

    Google Scholar 

  • Ball MC, Critchley C (1982) Photosynthetic responses to irradiance by the Grey Mangrove, Avicennia marina, grown under different light regimes. Plant Physiol 70:1101–1106. doi:10.1104/pp.70.4.1101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ball MC, Cowan IR, Farquhar GD (1988) Maintenance of leaf temperature and the optimization of carbon gain in relation to water loss in a tropical mangrove forest. Aust J Plant Physiol 15(263):276. doi:10.1071/PP9880263

    Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504. doi:10.1007/BF00402983

    Article  PubMed  Google Scholar 

  • Burritt DJ, Mackenzie S (2003) Antioxidant metabolism during acclimation of Begonia x erythrophylla to high light levels. Ann Bot 91:783–794. doi:10.1093/aob/mcg076

    Article  CAS  PubMed  Google Scholar 

  • Caemmerer SV, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. doi:10.1007/BF00384257

    Article  Google Scholar 

  • Campbell CD, Sage RF, Kocacinar F, Way DA (2005) Estimation of the whole-plant CO2 compensation point of Tobacco (Nicotiana tabacum L.). Glob Change Biol 11:1956–1967. doi:10.1111/j.1365-2486.2005.01045.x

    Google Scholar 

  • Cheeseman JM, Herendeen LB, Cheeseman AT, Clough BF (1997) Photosynthesis and photoprotection in mangroves under field conditions. Plant Cell Environ 20:579–588. doi:10.1111/j.1365-3040.1997.00096.x

    Article  CAS  Google Scholar 

  • Close DC, Beadle CL, Holz GK, Ravenwood IC (1999) A photobleaching event at the North Forest Products’ Somerset nursery reduces growth of Eucalyptus globulus seedlings. Tasforests 11:59–67

    Google Scholar 

  • Clough B (1998) Mangrove forest productivity and biomass accumulation in Hinchinbrook Channel, Australia. Mangroves Salt Marshes 2:191–198. doi:10.1023/A:1009979610871

    Article  Google Scholar 

  • Dai Y, Shen Z, Liu Y, Wang L, Hannaway D, Lu H (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot 65:177–182. doi:10.1016/j.envexpbot.2008.12.008

    Article  CAS  Google Scholar 

  • Evans JR (1989) Partition of nitrogen between and within leaves grown under different irradiances. Aust J Plant Physiol 16:533–548. doi:10.1071/PP9890533

    Article  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. doi:10.1016/S0304-4165(89)80016-9

    Article  CAS  Google Scholar 

  • Gray GR, Chauvin LP, Sarhan F, Huner NPA (1997) Cold acclimation and freezing tolerance: a complex interaction of light and temperature. Plant Physiol 114:467–474. doi:10.1104/pp.114.2.467

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoppe-Speera SCL, Adams JB, Rajkaran A, Bailey D (2011) The response of the red mangrove Rhizophora mucronata Lam. to salinity and inundation in South Africa. Aquatic Bot 95:71–76. doi:10.1016/j.aquabot.2011.03.006

    Article  Google Scholar 

  • Huang D, Wu L, Chen JR, Dong L (2011) Morphological plasticity, photosynthesis and chlorophyll fluorescence of Athyrium pachyphlebium at different shade levels. Photosynthetica 49(4):611–618. doi:10.1007/s11099-011-0076-1

    Article  CAS  Google Scholar 

  • Hunt D (2003) Measurements of photosynthesis and respiration in plants. Physiol Plant 117:314–325. doi:10.1034/j.1399-3054.2003.00055.x

    Article  CAS  PubMed  Google Scholar 

  • Janzen DH (1985) Mangroves: where’s the understory? J Trop Ecol 1:89–92. doi:10.1017/S0266467400000122

    Article  Google Scholar 

  • Kao WY, Tsai HC (1999) The photosynthesis and chlorophyll a fluorescence in seedlings of Kandelia candel (L.) Druce grown under different nitrogen and NaCl controls. Photosynthetica 37(3):405–412. doi:10.1023/A:1007103709598

    Article  CAS  Google Scholar 

  • Kao WY, Shih CN, Tsai TT (2004) Sensitivity to chilling temperatures and distribution differ in the mangrove species Kandelia candel and Avicennia marina. Tree Physiol 24:859–864. doi:10.1093/treephys/24.7.859

    Article  PubMed  Google Scholar 

  • Khan SR, Rose R, Haase DL, Sabin TE (2000) Effects of shade on morphology, chlorophyll concentration, and chlorophyll fluorescence of four Pacific Northwest conifer species. New For 19:171–186. doi:10.1023/A:1006645632023

    Article  Google Scholar 

  • Kitao M, Utsugi H, Kuramoto S, Tabuchi R, Fujimoto K, Lihpai S (2003) Light-dependent photosynthetic characteristics indicated by chlorophyll fluorescence in five mangrove species native to Pohnpei Island. Micronesia Physiol Plant 117:376–382. doi:10.1034/j.1399-3054.2003.00042.x

    Article  CAS  Google Scholar 

  • Kitaya Y, Sumiyoshi M, Kawabata Y, Monji N (2002) Effect of submergence and shading of hypocotyls on leaf conductance in young seedlings of the mangrove Rhizophora stylosa. Trees 16:147–149. doi:10.1007/s00468-002-0165-7

    Article  CAS  Google Scholar 

  • Krause GH (1994) Photoinhibition induced by low temperature. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the Field. Bios Scientific, Oxford, pp 331–348

    Google Scholar 

  • Krauss KW, Allen JA (2003) Influences of salinity and shade on seedling photosynthesis and growth of two mangrove species, Rhizophora mangle and Bruguiera sexangula, introduced to Hawaii. Aquatic Bot 77:311–324. doi:10.1016/j.aquabot.2003.08.004

    Article  Google Scholar 

  • Ku SB, Edwards GE (1977) Oxygen inhibition of photosynthesis. II. Kinetic characteristics as affected by temperature. Plant Physiol 59:991–999. doi:10.1104/pp.59.5.991

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Litchtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3):379–393. doi:10.1007/s11099-005-0062-6

    Article  Google Scholar 

  • Liu J, Zhou G, Yang C, Ou Z, Peng C (2007) Responses of chlorophyll fluorescence and xanthophyll cycle in leaves of Schima superba Gardn. & Champ. and Pinus massoniana Lamb. to simulated acid rain at Dinghushan Biosphere Reserve, China. Acta Physiol Plant 29:33–38. doi:10.1007/s11738-006-0005-2

    Article  Google Scholar 

  • Loh FCW, Grabosky JC, Bassuk NL (2002) Using the SPAD 502 meter to assess chlorophyll and nitrogen content of Benjamin fig and cottonwood leaves. Hort Technol 12(4):682–686

    CAS  Google Scholar 

  • Macnae W (1969) Zonation within mangroves associated with estuaries in north Queensland. In: Lauff GE (ed) Estuaries. AAAS, Washington, DC, pp 432–441

    Google Scholar 

  • Majláth I, Szalai G, Soós V, Sebestyén E, Balázs E, Vanková R, Dobrev PI, Tari D, Tandori J, Janda T (2012) Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. Physiol Plant 145:296–314. doi:10.1111/j.1399-3054.2012.01579.x

    Article  PubMed  Google Scholar 

  • Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynth Res 46:467–472. doi:10.1007/BF00032301

    Article  CAS  PubMed  Google Scholar 

  • Martin CE, Hsu RCC, Lin TC (2010) Sun/shade adaptations of the photosynthetic apparatus of Hoya carnosa, an epiphytic CAM vine, in a subtropical rain forest in northeastern Taiwan. Acta Physiol Plant 32:575–581. doi:10.1007/s11738-009-0434-9

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  CAS  PubMed  Google Scholar 

  • McLeod E, Salm RV (2006) Managing mangroves for resilience to climate change. The International Union for the Conservation of Nature and Natural, Gland, Switzerland, p 63

  • Moore RT, Miller PC, Ehlinger J, Lawrence W (1973) Seasonal trends in gas exchange characteristics of three mangrove species. Photosynthetica 7:387–394

    Google Scholar 

  • Naidoo G, Tuffers AV, Willert DJ (2002) Changes in gas exchange and chlorophyll fluorescence characteristics of two mangroves and a mangrove associate in response to salinity in the natural environment. Trees 16:140–146. doi:10.1007/s00468-001-0134-6

    Article  CAS  Google Scholar 

  • Okimoto Y, Nose A, Katsuta Y, Tateda Y, Agarie S, Ikeda K (2007) Gas exchange analysis for estimating net CO2 fixation capacity of mangrove (Rhizophora stylosa) forest in the mouth of river Fukido, Ishigaki Island, Japan. Plant Prod Sci 10(3):303–313. doi:10.1626/pps.10.303

    Article  CAS  Google Scholar 

  • Okimoto Y, Nose A, Ikeda K, Agarie S, Oshima K, Tateda Y, Ishii T, Nhan DD (2008) An estimation of CO2 fixation capacity in mangrove forest using two methods of CO2 gas exchange and growth curve analysis. Wetlands Ecol Manag 16:155–171. doi:10.1007/s11273-007-9062-6

    Article  Google Scholar 

  • Ong JE, Gong WK, Clough BF (1995) Structure and productivity of a 20-year-old stand of Rhizophora apiculata Bl. mangrove forest. J Biogeogr 22:417–424

    Article  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: molecular mechanisms to the field. Bios Scientific, Oxford, pp 1–24

    Google Scholar 

  • Paquette A, Bouchard A, Cogliastro A (2007) Morphological plasticity in seedlings of three deciduous species under shelterwood under-planting management does not correspond to shade tolerance ranks. For Ecol Manag 241:278–287. doi:10.1016/j.foreco.2007.01.004

    Article  Google Scholar 

  • Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM (2010) Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. J Plant Physiol 167:1052–1060. doi:10.1016/j.jplph.2010.03.001

    Article  CAS  PubMed  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35:15–44. doi:10.1146/annurev.pp.35.060184.000311

    Article  CAS  Google Scholar 

  • Putra ETS, Zakaria W, Abdullah NAP, Saleh GB (2012) Stomatal morphology, conductance and transpiration of Musa sp. Cv. Rastali in relation to magnesium, boron and silicon availability. Am J Plant Physiol 7(2):84–96. doi:10.3923/ajpp.2012.84.96

    Article  CAS  Google Scholar 

  • Robakowski P (2005) Susceptibility to low-temperature photoinhibition in three conifers differing in successional status. Three Physiol 25:1151–1160

    Article  Google Scholar 

  • Sage RF, Reid CD (1994) Photosynthetic response mechanisms to environmental change in C3 plants. In: Wilkinson (ed) Plant-environment interactions. Marcel Dekker Inc, New York, pp 413–499

    Google Scholar 

  • Sawada S, Miyachi S (1974) Effects of growth temperature on photosynthetic carbon metabolism in green plants. I. Photosynthetic activities of various plants acclimatized to varied temperatures. Plant Cell Physiol 15:111–120

    CAS  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer-Verlag, Berlin, pp 49–70

    Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105. doi:10.1007/BF02861058

    Article  Google Scholar 

  • Smith TJ III (1987) Effects of light and intertidal position on seedling survival and growth in tropical tidal forests. J Exp Mar Biol Ecol 110:133–146. doi:10.1016/0022-0981(87)90024-4

    Article  Google Scholar 

  • Srivastava PBL, Guan SL, Muktar A (1988) Progress of crop in come Rhizophora stands before first thinning in Matang Mangrove Reserve of Peninsular Malaysia. Pertanika 11(3):365–374

    Google Scholar 

  • Takahashi S, Tamashiro A, Sakihama Y, Yamamoto Y, Kawamitsu Y, Yamasaki H (2002) High-susceptibility of photosynthesis to photoinhibition in the tropical plant Ficus microcarpa L. f. cv, Golden Leaves. BMC Plant Biol 2:1–8. doi:10.1186/1471-2229-2-2

    Article  Google Scholar 

  • Tezara W, Martianez D, Rengifo E, Herrera A (2003) Photosynthetic responses of the tropical spiny shrub Lycium nodosum (Solanaceae) to drought, soil salinity and saline spray. Ann Bot Lond 92:757–765. doi:10.1093/aob/mcg199

    Article  CAS  Google Scholar 

  • Wang’ondu, Virginia W (2010) Phenology of Rhizophora mucronata LAMK, Avicennia marina (FORSSK.) VIERH. and Sonneratia alba SM in natural and reforested mangrove forests at Gazi Bay, Kenya. Dissertation, University of Nairobi, School of Biological Sciences

  • White AT, Martosubroto P, Sadorra MSM (1989) The Coastal environmental profile of segara Anakan-Cilacap, South Java, Indonesia. ICLARM Technical Reports 25. International Center for Living Aquatic Resources Management, Manila, Philippines, p 82

  • Whitten T, Damanik SJ, Anwar J, Hisyam N (2000) The ecology of Sumatra. The ecology of Indonesia series vol 1, First Periplus Edition, Singapore

  • Wittman C, Aschan G, Pfanz H (2001) Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime. Basic Appl Ecol 2:145–154. doi:10.1078/1439-1791-00047

    Article  Google Scholar 

  • Xu F, Guo W, Wang R, Xu W, Du N, Wang Y (2009) Leaf movement and photosynthetic plasticity of black locust (Robinia pseudoacacia) alleviate stress under different light and water conditions. Acta Physiol Plant 31:553–563. doi:10.1007/s11738-008-0265-0

    Article  CAS  Google Scholar 

  • Xuan X, Wang Y, Ma S, Ye X (2011) Comparisons of stomatal parameters between normal and abnormal leaf of Bougainvillea spectabilis Willd. Afr J Biotechnol 10:6973–6978. doi:10.5897/AJB10.2196

    Google Scholar 

  • Zhou J, Zhou J Jr, Wu B, Qin P, Qi A (2010) Physiological factors for tolerance of Kosteletzkya virginica (L.) Presl to one-instar bollworms of Helicoverpa armigera (Hubner). Acta Physiol Plant 32:519–529. doi:10.1007/s11738-009-0429-6

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by The Rendai-Student Supporting Program 2011-2012, United Graduate School of Agricultural Sciences, Kagoshima University, Japan. The authors are grateful to Directorate General of Higher Education (DIKTI), Republic of Indonesia for the PhD Grant of T. Z. Ulqodry.

Author information

Authors and Affiliations

  1. Faculty of Agriculture, Saga University, 1 Honjo-machi, Saga, 840-8502, Japan

    Tengku Zia Ulqodry, Fumiko Matsumoto, Yosuke Okimoto, Akihiro Nose & Shao-Hui Zheng

  2. The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan

    Tengku Zia Ulqodry

  3. Department of Marine Science, Sriwijaya University, South Sumatera, 30662, Indonesia

    Tengku Zia Ulqodry

  4. Center for International Forestry Research, Bogor, Indonesia

    Yosuke Okimoto

Authors
  1. Tengku Zia Ulqodry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fumiko Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yosuke Okimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akihiro Nose
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shao-Hui Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akihiro Nose.

Additional information

Communicated by Z. Gombos.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ulqodry, T.Z., Matsumoto, F., Okimoto, Y. et al. Study on photosynthetic responses and chlorophyll fluorescence in Rhizophora mucronata seedlings under shade regimes. Acta Physiol Plant 36, 1903–1917 (2014). https://doi.org/10.1007/s11738-014-1566-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1566-0

Keywords

Search

Navigation