, Volume 33, Issue 1, pp 11–22 | Cite as

Light deficiency and waterlogging affect chlorophyll metabolism and photosynthesis in Magnolia sinostellata

  • Qin Yu
  • Yamei ShenEmail author
  • Qianying Wang
  • Xingli Wang
  • Lijie Fan
  • Yaling Wang
  • Shouzhou Zhang
  • Zhigao Liu
  • Mingru Zhang
Original Article


Key message

In Magnolia sinostellata plants grown under shading and waterlogging conditions, solar noon PFD level of 1050 ± 30 µmol·m− 2·s− 1 and running water combined treatment (L1W2) triggers changes in chlorophyll metabolism and photosynthesis, which benefits growth of this endangered species.


Magnolias are widely used as ornamental plants in cities, but they are facing extinction in the wild. It has been hypothesized that shading from trees in the upper canopy and stress from waterlogging conditions reduce their survival rates. To test this hypothesis, we grew 2-year-old Magnolia sinostellata seedlings either under natural light level (solar noon PFD of 1400 ± 28 µmol·m− 2·s− 1) and normal watering conditions (watered every 3 days) (control, CK) or reduced light levels (L1 1050 ± 30 µmol·m− 2·s− 1; L2 700 ± 27 µmol·m− 2·s− 1 and L3 490 ± 25 µmol·m− 2·s− 1) in combination with two types of waterlogging scenarios: still water treatment (W1, water level kept at 2 cm above soil surface) or running water treatment (W2, constantly irrigated via drip-irrigation). Measurements of chlorophyll content, gas exchange, and relative expression of genes involved in chlorophyll synthesis revealed that chlorophyll content, net photosynthetic rate, stomatal conductance, and transpiration rate were significantly higher in L1W2 treatment than the control or any of the other treatment examined, whereas the intercellular CO2 concentration was lower under the L1W2 treatment. The expression levels of genes involved in chlorophyll biosynthesis were higher under L1W2 than CK conditions, but lower under L1W1, L2W1, L2W2, L3W1, and L3W2 treatment. These results suggest that L1W2 condition is most suitable for chlorophyll synthesis and photosynthesis of M. sinostellata. This study provides new insights into the physiology and development of endangered plants and useful guidance for conservation efforts aimed at protecting wild magnolia species.


Magnolia sinostellata Chlorophyll Photosynthesis Shading and water treatments 



We are thankful to the editor and two anonymous reviewers for their comments on this paper. We thank Lailiang Cheng (Department of Horticulture, Cornell University, USA) for careful advising of this article. We thank Dr. Bin Dong, Chao Zhang for sharing knowledge about gene sequence analysis. This work was financially supported by the National Natural Science Foundation of China (31400599); the 13th 5-Year-Plan for Floriculture Special Breeding of Zhejiang Province, China (2016C02056-12); and the Public Welfare Forestry Industry Project of State Forestry Administration, China (201504322).

Author contribution statement

QY and YS were the equal chief scientist in this study, designed the experiments, conducted statistical analysis, and wrote the manuscript; QW, XW and LF, major participants in this study, were responsible for data collection; YW, SZ, ZL and MZ, major participants in this study, were responsible for manuscript revision and language improvement.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2018_1753_MOESM1_ESM.tif (719 kb)
The structure of photosynthesis system (TIF 719 KB)
468_2018_1753_MOESM2_ESM.docx (15 kb)
The relative expression of genes involved in Calvin Cycle (DOCX 15 KB)


  1. Aarti PD, Tanaka R, Tanaka A (2006) Effects of oxidative stress on chlorophyll biosynthesis in cucumber (Cucumis sativus) cotyledons. Physiol Plant 128:186–197CrossRefGoogle Scholar
  2. Aleric KM, Kirkman LK (2005) Growth and photosynthetic responses of the federally endangered shrub, Lindera melissifolia (Lauraceae), to varied light environments. Am J Bot 92:682–689CrossRefGoogle Scholar
  3. Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137:263–273CrossRefGoogle Scholar
  4. Aranda I, Castro L, Pardos M, Gil L, Pardos JA (2005) Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak (Quercus suber L.) seedlings. For Ecol Manage 210:117–129CrossRefGoogle Scholar
  5. Arjenaki FG, Jabbar R, Morshed A (2012) Evaluation of drought stress on relative water content, chlorophyll content and mineral elements of wheat (Triticum aestivum L.) varieties. Int J Agric Crop Sci 4:726–729Google Scholar
  6. Bartholomeus RP, Witte JPM, van Bodegom PM, van Dam JC, Aerts R (2011) Climate change threatens endangered plant species by stronger and interacting water-related stresses. J Geophys Res 116:116–120CrossRefGoogle Scholar
  7. Cheng Y, Dong Y, Yan H, Ge W, Shen C, Guan J, Liu L, Zhang Y (2012) Effects of 1-MCP on chlorophyll degradation pathway-associated genes expression and chloroplast ultrastructure during the peel yellowing of Chinese pear fruits in storage. Food Chem 135:415–422CrossRefGoogle Scholar
  8. Dai YJ, Shen ZG, Liu Y, Wang LL, Hannaway D, Lu HF (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot 65:177–182CrossRefGoogle Scholar
  9. Dalal VK, Tripathy BC (2012) Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant Cell Environ 35:1685–1703CrossRefGoogle Scholar
  10. Farquhar GD, Caemmerer SV (1982) Modeling of photosynthetic response to environmental conditions. Encycl Plant Physiol 12B:317–325CrossRefGoogle Scholar
  11. Gaubier P, Wu HJ, Laudié M, Delseny M, Grellet F (1995) A chlorophyll synthetase gene from Arabidopsis thaliana. Mol Gen Genet 249:58–64CrossRefGoogle Scholar
  12. Ge Y, Lu YJ, Liao JX, Guan BH, Chang J (2004) Photosynthetic parameters of Mosla hangchowensis and M. dianthera as affected by soil moisture. Photosynthetica 42:387–391CrossRefGoogle Scholar
  13. Hasemidezfouli A, Herbert SJ (1992) Intensifying plant density response of corn with artificial shade. Agron J 84:547–551CrossRefGoogle Scholar
  14. Hörtensteiner S (2013) Update on the biochemistry of chlorophyll breakdown. Plant Mol Biol 82:505–517CrossRefGoogle Scholar
  15. Ikegami A, Yoshimura N, Motohashi K, Takahashi S, Romano PG, Hisabori T, Takamiya K, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282:19282–19291CrossRefGoogle Scholar
  16. Kim J, Eichacker L, Rudiger W, Mullet JE (1994) Chlorophyll regulates accumulation of the plastid- encoded chlorophyll proteins P700 and D1 by increasing apoprotein stability. Plant Physiol 104:907–916CrossRefGoogle Scholar
  17. Li NN, Yang YP, Ye JH, Lu JL, Zheng XQ, Liang YR (2016) Effects of sunlight on gene expression and chemical composition of light-sensitive albino tea plant. Plant Growth Regul 78:253–262CrossRefGoogle Scholar
  18. Liao JX, Ge Y, Guan BH, JIiang YP, Chang J (2006) Photosynthetic characteristics and growth of Mosla hangchowensis and M. dianthera under different irradiances. Biol Plant 50:737–740CrossRefGoogle Scholar
  19. Liu p, Yang YS, Xu GD, Hao CY (2006) Physiological response of rare and endangered seven-son-flower (Heptacodium miconioides) to light stress under habitat fragmentation. Environ Exp Bot 57:32–40CrossRefGoogle Scholar
  20. Liu D, Kong DD, Fu XK, Ali B, Xu L, Zhou WJ (2016) Influence of exogenous 5-aminolevulinic acid on chlorophyll synthesis and related gene expression in oilseed rape de-etiolated cotyledons under water-deficit stress. Photosynthetica 54:468–474CrossRefGoogle Scholar
  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408CrossRefGoogle Scholar
  22. Malavasi UC, Malavasi MM (2001) Leaf characteristics and chlorophyll concentration of Schyzolobium parahybum and Hymenaea stilbocarpa seedlings grown in different light regimes. Tree Physiol 21:701–703CrossRefGoogle Scholar
  23. Nagata N, Tanaka R, Satoh S, Tanaka A (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17:233–240CrossRefGoogle Scholar
  24. Nepal S, Ojha BR, Meador AJS, Gaire SP, Shilpakar C (2014) Effect of gamma rays on germination and photosynthetic pigments of maize (Zea Mays L.) Inbreds. Int J Res 111:511–525Google Scholar
  25. Ohmiya A, Hirashima M, Yagi M, Tanase K, Yamamizo C (2014) Identification of genes associated with chlorophyll accumulation in flower petals. PLoS One 9:e113738CrossRefGoogle Scholar
  26. Osório ML, Osório J, Romano A (2012) Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought. Photosynthetica 51:75–84CrossRefGoogle Scholar
  27. Quinet M, Descamps C, Coster Q, Lutts S, Jacquemart AL (2015) Tolerance to water stress and shade in the invasive Impatiens parviflora. Int J Plant Sci 176:848–858CrossRefGoogle Scholar
  28. Rodoni S, Muhlecker W, Anderl M, Moser D, Krautler B, Thomas H, Matile P, Hortensteiner S (1997) Chlorophyll breakdown in senescent chloroplasts (cleavage of pheophorbide a in two enzymic steps). Plant Physiol 115:669–676CrossRefGoogle Scholar
  29. Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186CrossRefGoogle Scholar
  30. Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J 57:120–131CrossRefGoogle Scholar
  31. Shen YM, Meng D, McGrouther K, Zhang JH, Cheng LL (2017) Efficient isolation of Magnolia protoplasts and the application to subcellular localization of MdeHSF1. Plant Methods 13:44CrossRefGoogle Scholar
  32. Sun JL, Sui XL, Huang HY, Wang SH, Wei YX, Zhang ZX (2014) Low light stress down-regulated Rubisco gene expression and photosynthetic capacity during cucumber (Cucumis sativus L.) leaf development. J Integrative Agr 13:997–1007CrossRefGoogle Scholar
  33. Suzuki YJ, Makino A (2013) Translational downregulation of RBCL is operative in the coordinated expression of Rubisco genes in senescent leaves in rice. J Exp Bot 64:1145–1152CrossRefGoogle Scholar
  34. Suzuki Y, Ohkubo M, Hatakeyama H, Ohashi K, Yoshizawa R, Kojima S, Hayakawa T, Yamaya T, Mae T, Makino A (2007) Increased Rubisco content in transgenic rice transformed with the ‘sense’ rbcS gene. Plant Cell Physiol 48:626–637CrossRefGoogle Scholar
  35. Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of Photosystem II from photodamage. Biochim Biophys Acta 1708:352–361CrossRefGoogle Scholar
  36. Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255CrossRefGoogle Scholar
  37. Wang YL, Ejder E, Yang JF, Liu R, Ye LM, He ZC, Zhang SZ (2013) Magnolia sinostellata and relatives (Magnoliaceae). Phytotaxa 154:47–58CrossRefGoogle Scholar
  38. Yan C, Wang ZS, An SQ, Chen SN, Na W, Lu CM (2008) Differences in photosynthetic capacity among different diameter-classes of Parrotia subaequalis populations and their implications to regeneration limitation. Acta Ecol Sin 28:4153–4161Google Scholar
  39. Yin Z, Zhang Z, Deng D, Chao M, Gao Q, Wang Y, Yang Z, Bian Y, Hao D, Xu C (2014) Characterization of Rubisco activase genes in maize: an α-isoform gene functions alongside a β-isoform gene. Plant Physiol 164:2096–2106CrossRefGoogle Scholar
  40. Yu ZZ, Chen XX, Lu L, Liu XY, Yin H, Shen YM (2015) Distribution and community structure of Magnolia sinostellata. J Zhejiang For Sci Tech 35:47–52Google Scholar
  41. Zhang ZJ, Shi L, Zhang JZ, Zhang CY (2004) Photosynthesis and growth responses of Parthenocissus quinquefolia (L.) Planch to soil water availability. Photosynthetica 42:87–92CrossRefGoogle Scholar
  42. Zhang LD, Zhang LX, Sun JL, Zhang ZX, Ren HZ, Sui XL (2013) Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Sci Hortic 161:81–87CrossRefGoogle Scholar
  43. Zhang YJ, Yan F, Gao H, Xu YZ, Guo YY, Wang EJ, Li YH, Xie ZK (2015) Chlorophyll content, leaf gas exchange and growth of oriental lily as affected by shading. Russ J Plant Physiol 62:334–339CrossRefGoogle Scholar
  44. Zhang K, Liu ZY, Shan XF, Li CY, Tang XY, Chi MY, Feng H (2016) Physiological properties and chlorophyll biosynthesis in a Pak-choi (Brassica rapa L. ssp. chinensis) yellow leaf mutant, pylm. Acta Physiol Plant 39:22CrossRefGoogle Scholar
  45. Zhou W, Juneau P, Qiu B (2006) Growth and photosynthetic responses of the bloom-forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere 65:1738–1746CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Qin Yu
    • 1
  • Yamei Shen
    • 1
    Email author
  • Qianying Wang
    • 1
  • Xingli Wang
    • 1
  • Lijie Fan
    • 1
  • Yaling Wang
    • 2
  • Shouzhou Zhang
    • 3
  • Zhigao Liu
    • 1
  • Mingru Zhang
    • 1
  1. 1.School of Landscape and ArchitectureZhejiang A&F UniversityLin’anChina
  2. 2.Xi’an Botanical Garden of Shaanxi Academy of ScienceXi’anChina
  3. 3.Shenzhen Fairy Lake Botanical GardenShenzhenChina

Personalised recommendations