Acta Physiologiae Plantarum

, 37:235 | Cite as

Changes in photosynthesis of alpine plant Saussurea superba during leaf expansion

Original Article
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Abstract

The native alpine plant Saussurea superba is widely distributed in Qinghai–Tibetan Plateau regions. The leaves of S. superba grow in whorled rosettes, and are horizontally oriented to maximize sunlight exposure. Experiments were conducted in an alpine Kobresia humilis meadow near Haibei Alpine Meadow Ecosystem Research Station (37°29′–37°45′N, 101°12′–101°33′E; alt. 3200 m). Leaf growth, photosynthetic pigments and chlorophyll fluorescence parameters were measured in expanding leaves of S. superba. The results indicate that leaf area increased progressively from inner younger leaves to outside fully expanded ones, and then slightly decreased in nearly senescent leaves, due to early unfavorable environmental conditions, deviating from the ordinary growth pattern. The specific leaf area decreased before leaves were fully expanded, and the leaf thickness was largest in mature leaves. There were no significant changes in the content of chlorophylls (Chl) and carotenoids (Car), but the ratios of Chl a/b and Car/Chl declined after full expansion of the leaves. The variation of Chl a/b coincided well with changes in photochemical quenching (q P) and the fraction of open PSII reaction centers (q L). The maximum quantum efficiency of PSII photochemistry after 5 min dark relaxation (F (v)/F (m)) continuously increased from younger leaves to fully mature leaves, suggesting that mature leaves could recover more quickly from photoinhibition than younger leaves. The light-harvesting capacity was relatively steady during leaf expansion, as indicated by the maximum quantum efficiency of open PSII centers (\(F_{\text{v}}^{{\prime }}\)/\(F_{\text{m}}^{{\prime }}\)). UV-absorbing compounds could effectively screen harmful solar radiation, and are a main protection way on the photosynthetic apparatus. The decline of q P and q L during maturation, together with limitation of quantum efficiency of PSII reaction centers (L (PFD)), shows a decrease of oxidation state of QA in PSII reaction centers under natural sunlight. Furthermore, light-induced (Φ NPQ) and non-light-induced quenching (Φ NO) were consistent with variation of L (PFD). It is concluded that the leaves of S. superba could be classified into four functional groups: young, fully expanded, mature, and senescent. Quick recovery from photoinhibition was correlated with protection by screening pigments, and high level of light energy trapping was correlated with preservation of photosynthetic pigments. Increasing of Φ NPQ and Φ NO during leaves maturation indicates that both thermal dissipation of excessive excitation energy in safety and potential threat to photosynthetic apparatus were strengthened due to the declination of q P and q L, and enhancement of L (PFD).

Keywords

Alpine plant Chlorophyll fluorescence parameters Leaf growth Photosynthetic pigments Qinghai–Tibetan Plateau Saussurea superba 

Abbreviations

SLA

Specific leaf area

LWR

Ratio of dry to fresh weight of leaves

Chl

Chlorophylls

Car

Carotenoids

Chl a/b

Ratio of chlorophyll a to chlorophyll b

Car/Chl

Ratio of carotenoids to chlorophylls

qP

Photochemical quenching coefficient

NPQ

Non-photochemical quenching coefficient

qL

Fraction of opened PSII reaction centers

F(v)/F(m)

Maximum quantum efficiency of PSII photochemistry after 5 min dark relaxation

\(F_{\text{v}}^{{\prime }}\)/\(F_{\text{m}}^{{\prime }}\)

Maximum quantum efficiency of PSII photochemistry at given light

L(PFD)

Relative limitation of quantum efficiency of PSII reaction centers

ΦNPQ

Quantum yield of light-induced PSII regulatory energy dissipation

ΦNO

Quantum yield of non-light-induced PSII non-regulatory energy dissipation

ΦPSII

Actual quantum yield of PSII photochemistry

QA

Primary quinone electron acceptor of PSII

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (30670307), the Key Plan of International Cooperation Research in Sciences and Techniques (2002CB714006), and the Natural Science Foundation of Qinghai Province (2013-Z-915). We thank Professor Lars Olof Björn for critical reading and editing of this manuscript.

References

  1. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedCentralCrossRefPubMedGoogle Scholar
  2. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefPubMedGoogle Scholar
  3. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621CrossRefPubMedGoogle Scholar
  4. Bilger W, Björkman O (1990) Role of the xanthophyll cycle protoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185CrossRefPubMedGoogle Scholar
  5. Catský J, Šesták Z (1996) Photosynthesis during leaf development. In: Pessarakli M (ed) Handbook of photosynthesis. Marcel Dekker, New York, pp 633–660Google Scholar
  6. Cha-um S, Takabe T, Kirdmanee C (2010) Osmotic potential, photosynthetic abilities and growth characters of oil palm (Elaeis guineensis Jacq.) seedlings in responses to polyethylene glycol-induced water deficit. Afr J Biotechnol 9:6509–6516Google Scholar
  7. Choinski JS Jr, Ralph P, Eamus D (2003) Changes in photosynthesis during leaf expansion in Corymbia gummifera. Aust J Bot 51:111–118CrossRefGoogle Scholar
  8. Day TA, Neale PJ (2002) Effects of UV-B radiation on terrestrial and aquatic primary producers. Annu Rev Ecol Syst 33:371–396CrossRefGoogle Scholar
  9. Day TA, Howells BW, Rice WJ (1994) Ultraviolet absorption and epidermal-transmittance spectra in foliage. Physiol Plant 92:207–218CrossRefGoogle Scholar
  10. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626CrossRefGoogle Scholar
  11. Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21CrossRefPubMedGoogle Scholar
  12. Demmig-Adams B, Adams WW, Barke DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:254–264Google Scholar
  13. Demmig-Adams B, Cohu CM, Muller O, Adams WW (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to season. Photosynth Res 113:75–88CrossRefPubMedGoogle Scholar
  14. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1980) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101CrossRefGoogle Scholar
  15. Dillenburg LR, Sullivan JH, Teramura AH (1995) Leaf expansion and development of photosynthetic capacity and pigments in Liquidambar styraciflua (Hammamelidaceae). Am J Bot 82:433–440Google Scholar
  16. Dodd IC, Critchley C, Woodall GS, Stewart GR (1998) Photoinhibition in differently coloured juvenile leaves of Syzygium species. J Exp Bot 49:1437–1445CrossRefGoogle Scholar
  17. Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767CrossRefGoogle Scholar
  18. Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smimoff N, Asami T, Davies WJ, Jones AM, Baker NR, Mullineaux PM (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–2162PubMedCentralCrossRefPubMedGoogle Scholar
  19. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  20. Holleboom C-P, Walla PJ (2014) The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting. Photosynth Res 119:215–221CrossRefPubMedGoogle Scholar
  21. Jiang CD, Li PM, Gao HY, Zou Q, Jiang GM, Li LH (2005) Enhanced photoprotection at the early stages of leaf expansion in field-grown soybean plants. Plant Sci 168:911–919CrossRefGoogle Scholar
  22. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218CrossRefPubMedGoogle Scholar
  23. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  24. Middleton EM, Teramura AH (1993) The role of flavonol glycoside and carotenoids in protecting soybean from ultraviolet-B damage. Plant Physiol 103:475–481Google Scholar
  25. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566PubMedCentralCrossRefPubMedGoogle Scholar
  26. Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92PubMedCentralCrossRefPubMedGoogle Scholar
  27. Osório ML, Osório J, Romano A (2013) Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought. Photosynthetica 51:75–84CrossRefGoogle Scholar
  28. Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components: calculation of q P and F v′/F m′ without measuring F o′. Photosynth Res 54:135–142CrossRefGoogle Scholar
  29. Perez CEA, Rodrigues FÁ, Moreira WR, DaMatta FM (2014) Leaf gas exchange and chlorophyll a fluorescence in wheat plants supplied with silicon and infected with Pyricularia oryzae. Biochem Cell Biol 104:143–149Google Scholar
  30. Quick WP, Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim Biophys Acta 977:287–296CrossRefGoogle Scholar
  31. Rikkinen J (1995) What’s behind the pretty colours? A study on the photobiology of lichen. Bryobothera 4:231–239Google Scholar
  32. Sáez PL, Bravo LA, Latsague MI, Toneatti MJ, Sánchez-Olate M, Ríos DG (2013) Light energy management in micropropagated plants of Castanea sativa, effects of photoinhibition. Plant Sci 201:12–24CrossRefPubMedGoogle Scholar
  33. Shi SB, Han F, Ben GY (1997) Midday depression in net photosynthetic rate of plant community in alpine Kobresia humilis meadow. Acta Phytoecol Sin 23:405–409 (in Chinese with English abstract) Google Scholar
  34. Shi SB, Ben GY, Han F, Li YN, Shen ZX (2001a) Plant growth analysis of Kobresia humilis meadow community in Qing-Zang plateau regions. Acta Ecol Sin 21:871–876 (in Chinese with English abstract) Google Scholar
  35. Shi SB, Han F, Li HY (2001b) Midday depression of photosynthesis of Gentiana straminea and Saussurea superba in alpine Kobresia humilis meadow. Acta Phytophysiol Sin 27:123–128 (in Chinese with English abstract) Google Scholar
  36. Shi SB, Zhu WY, Li HM, Zhou DW, Han F, Zhao XQ, Tang YH (2004) Photosynthesis of Saussurea superba and Gentiana straminea is not reduced after long-term enhancement of UV-B radiation. Environ Exp Bot 51:75–83CrossRefGoogle Scholar
  37. Solovchenko A, Lukyanov A, Solovchenko O, Didi-Cohen S, Boussiba S, Khozin-Goldberg I (2014) Interactive effects of salinity, high light, and nitrogen starvation on fatty acid and carotenoid profiles in Nannochloropsis oceanica CCALA 804. Eur J Lipid Sci Technol 116:1–10CrossRefGoogle Scholar
  38. Sperdouli I, Moustakas M (2012) Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress. Acta Physiol Plant 34:1267–1276CrossRefGoogle Scholar
  39. Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215CrossRefPubMedGoogle Scholar
  40. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiol 144:307–313CrossRefGoogle Scholar
  41. Xu DQ (2002) Photosynthetic efficiency. Shanghai Scientific and Technical Press, Shanghai, pp 29–37 (in Chinese) Google Scholar
  42. Yu BH, Lu CH (2011) Assessment of ecological vulnerability on the Tibetan Plateau. Geogr Res 30:2289–2294 (in Chinese with English abstract) Google Scholar
  43. Zhao XQ, Zhou XM (1999) Ecological basis of Alpine meadow ecosystem management in Tibet: Haibei Alpine Meadow Ecosystem Research Station. Ambio 28:642–647Google Scholar
  44. Zhu GL (1990) Plant physiological experiment. Peking University Press, Beijing, pp 51–54 (in Chinese) Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2015

Authors and Affiliations

  1. 1.Northwest Institute of Plateau BiologyChinese Academy of SciencesXiningPeople’s Republic of China
  2. 2.School of Life ScienceSun-Yat-Sen UniversityGuangzhouPeople’s Republic of China

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