Advertisement

The Role of Leaf Movements for Optimizing Photosynthesis in Relation to Environmental Variation

  • Erik T. NilsenEmail author
  • Irwin N. ForsethJr
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)

Summary

There is an amazing array of leaf movements among plants, elicited by a wide variety of environmental signals. Leaf movements may occur over developmental time scales, involving growth processes, or over the scale of milliseconds involving rapid depolarization of membranes and ion fluxes. This chapter covers primarily leaf movements in response to light, although mechanical stimuli, temperature, and water are also discussed. The focus on phototropism, heliotropism, and thermonasty is due to the large effects these movements have on rates of photosynthesis. Heliotropism, whether it is due to differential growth on opposite sides of a plant stem, or turgor changes within a motor organ such as a pulvinus, has direct and large effects on light interception. Diaheliotropic, paraheliotropic, or a combination of the two movements may act to increase photosynthesis by increasing light interception, or optimize resource use efficiency by modulating incident light at intermediate levels. Paraheliotropic and wilting movements are major adaptive mechanisms in response to water deficits, high light, high temperatures, or a combination of these stresses. Thermonastic movements have been shown to play a major role in reducing damage to the photosynthetic machinery during low temperature periods, or conversely in high temperature periods. Despite the mounting number of case studies, a comprehensive understanding of the signal cascades and regulatory genetic pathways controlling rapid, reversible leaf movements has yet to be accomplished. An understanding of the phylogeographic distribution of rapid leaf movements is also lacking. The presence of rapid leaf movements in a number of commercially important crop species suggests that incorporation and modification of these properties may have potential to improve both productivity and stress resistance in cultivated species.

Abbreviations

A

net photosynthesis rate (μmol CO2 m−2 s−1)

gs

stomatal conductance (mmol H2O m−2 s−1)

PPF

photosynthetic photon flux (μmol m−2 s−1)

WUE

water use efficiency (mol of CO2 gained mol−1 H2O lost)

E

transpiration (mmol H2O m−2 s−1)

Notes

Acknowledgments

For INF, this material is based upon work while serving at the National Science Foundation. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. For ETN, the work presented in this review was funded by the National Science Foundation and the American Rhododendron Society.

References

  1. Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2013) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117:31–44PubMedCrossRefPubMedCentralGoogle Scholar
  2. Adams WWIII, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WWIII, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment, advances in photosynthesis and respiration, vol 21. Springer, Dordrecht, pp 49–64CrossRefGoogle Scholar
  3. Adams WWIII, Muller O, Cohu CM, Demmig-Adams B (2014) Photosystem II efficiency and non-photochemical quenching in the context of source-sink balance. In: Demmig-Adams B, Garab G, Adams WW III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht, pp 503–529Google Scholar
  4. Alvarez JM, Rocha JF, Machado SR (2008) Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): structure in relation to function. Braz Arch Biol Tech 51:113–119CrossRefGoogle Scholar
  5. Amador-Vargas S, Dominguez M, Leon G, Maldonado B, Murillo J, Vides GL (2014) Leaf-folding response of a sensitive plant shows context-dependent behavioral plasticity. Plant Ecol 215:1445–1454CrossRefGoogle Scholar
  6. Arena C, Vitale L, De Santo AV (2008) Paraheliotropism in Robinia pseudoacacia L.: an efficient strategy to optimise photosynthetic performance under natural environmental conditions. Plant Biol 10:194–201PubMedCrossRefGoogle Scholar
  7. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190CrossRefGoogle Scholar
  8. Bao YJ, Nilsen ET (1988) The ecophysiological significance of leaf movements in Rhododendron maximum. Ecology 69:1578–1587CrossRefGoogle Scholar
  9. Berg V, Hsiao T (1986) Solar tracking: light avoidance induced by water stress in leaves of kidney bean seedlings in the field. Crop Sci 26:980–986CrossRefGoogle Scholar
  10. Bielenberg DG, Miller JD, Berg VS (2003) Paraheliotropism in two Phaseolus species: combined effects of photon flux density and pulvinus temperature, and consequences for leaf gas exchange. Environ Exp Bot 49:95–105CrossRefGoogle Scholar
  11. Bjorkman O, Powles SB (1981) Leaf movement in the shade species Oxalis oregana 1. Response to light level and light quality. In: Ebert JD (ed) Carnegie Institution of Washington year book, 1980/1981. Carnegie Institution of Washington, Washington, DC, pp 59–62Google Scholar
  12. Bruinsma J, Hasegawa K (1990) A new theory of phototropism – its regulation by a light induced gradient of auxin-inhibiting substances. Physiol Plant 79:700–704PubMedCrossRefGoogle Scholar
  13. Chen J, Moreau C, Liu Y, Kawaguchi M, Hofer J, Ellis N, Chen R (2012) Conserved genetic determinant of motor organ identity in Medicago truncatula and related legumes. Proc Natl Acad Sci U S A 109:11723–11728PubMedPubMedCentralCrossRefGoogle Scholar
  14. Close DC, Beadle CL (2006) Leaf angle responds to nitrogen supply in eucalypt seedlings. Is it a photoprotective mechanism? Tree Physiol 26:743–748PubMedCrossRefGoogle Scholar
  15. Corlett JE, Jones HG, Massacci A, Masojidek J (1994) Water deficit, leaf rolling and susceptibility to photoinhibition in field grown sorghum. Physiol Plant 92:423–430CrossRefGoogle Scholar
  16. Darwin C, Darwin F (1896) The power of movement in plants. D. D. Appelton and Company, New YorkGoogle Scholar
  17. de Pinto MC, Locato V, Paradiso A, De Gara L (2015) Role of redox homeostasis in thermotolerance under a climate change scenario. Ann Bot 116:487–496PubMedPubMedCentralCrossRefGoogle Scholar
  18. Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21PubMedCrossRefPubMedCentralGoogle Scholar
  19. Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485PubMedCrossRefGoogle Scholar
  20. Eapen D, Martinez JJ, Cassab GI (2015) Assays for root hydrotropism and response to water stress. Methods Mol Biol 1309:133–142PubMedCrossRefGoogle Scholar
  21. Ehleringer JR, Forseth IN (1980) Solar tracking by plants. Science 210:1094–1098PubMedCrossRefGoogle Scholar
  22. Ehleringer JR, Forseth IN (1989) Diurnal leaf movements and productivity in canopies. In: Russell G, Marshall B, Jarvis PG (eds) Plant canopies: their growth, form and function, pp 129--142. Cambridge University Press, CambridgeGoogle Scholar
  23. Ehleringer JR, Hammond SD (1987) Solar tracking and photosynthesis in cotton leaves. Agric For Meteorol 39:25–35CrossRefGoogle Scholar
  24. Ehleringer JR (1983) Ecophysiology of Amaranthus palmeri, a Sonoran Desert summer annual. Oecologia 57:107–112PubMedCrossRefGoogle Scholar
  25. Feistler AM, Habermann G (2012) Assessing the role of vertical leaves within the photosynthetic function of Styrax camporum under drought conditions. Photosynthetica 50:613–622CrossRefGoogle Scholar
  26. Forseth IN (1990) Function of leaf movement. In: Satter RL, Gorton HL, Vogelmann TC (eds) Current topics in plant physiology an American Society of Plant Physiologists Series V III. American Society of Plant Physiologists, Rockville, pp 238–261Google Scholar
  27. Forseth IN, Ehleringer JR (1980) Solar tracking response to drought in a desert annual. Oecologia 44:159–163PubMedCrossRefGoogle Scholar
  28. Forseth IN, Ehleringer JR (1982) Ecophysiology of 2 solar tracking desert winter annuals. 2. Leaf movements, water relations and microclimate. Oecologia 54:41–49PubMedCrossRefGoogle Scholar
  29. Forseth IN, Ehleringer JR (1983a) Ecophysiology of 2 solar tracking desert winter annuals. 4. Effects of leaf orientation on calculated daily carbon gain and water-use efficiency. Oecologia 58:10–18PubMedCrossRefGoogle Scholar
  30. Forseth IN, Ehleringer JR (1983b) Ecophysiology of 2 solar tracking desert winter annuals. 3. Gas-exchange responses to light, CO2 and vpd in relation to long-term drought. Oecologia 57:344–351PubMedCrossRefGoogle Scholar
  31. Forseth IN, Norman JM (1993) Modelling of solar irradiance, leaf energy budget and canopy photosynthesis. In: Hall DO, Scurlock JMO, Bolhar-Nordenkampf HR, Leegood RC, Long SP (eds) Photosynthesis and production in a changing environment: a field and laboratory manual. Springer, Berlin/Heidelberg, pp 207–219Google Scholar
  32. Forseth IN, Teramura AH (1987) Field photosynthesis, microclimate and water relations of an exotic temperate liana, Pueraria lobata, kudzu. Oecologia 71:262–267PubMedCrossRefGoogle Scholar
  33. Forterre Y (2013) Slow, fast and furious: understanding the physics of plant movements. J Exp Bot 64:4745–4760PubMedCrossRefGoogle Scholar
  34. Fu QA, Ehleringer JR (1989) Heliotropic leaf movements in common beans controlled by air temperature. Plant Physiol 91:1162–1167PubMedPubMedCentralCrossRefGoogle Scholar
  35. Greer DH, Thorpe MR (2009) Leaf photosynthetic and solar-tracking responses of mallow, Malva parviflora, to photon flux density. Plant Physiol Biochem 47:946–953PubMedCrossRefGoogle Scholar
  36. Gururani MA, Venkatesh J, Lam-Son Phan T (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320PubMedCrossRefGoogle Scholar
  37. Hasegawa T, Yamada K, Shigemori H, Goto N, Miyamoto K, Ueda J, Hasegawa K (2004) Isolation and identification of blue light-induced growth inhibitor from light-grown Arabidopsis shoots. Plant Growth Reg 44:81–86CrossRefGoogle Scholar
  38. Hashiguchi Y, Tasaka M, Morita MT (2013) Mechanism of higher plant gravity sensing. Am J Bot 100:91–100PubMedCrossRefGoogle Scholar
  39. Hashiguchi Y, Yano D, Nagafusa K, Kato T, Saito C, Uemura T et al (2014) A unique heat repeat-containing protein shoot gravitropism6 is involved in vacuolar membrane dynamics in gravity-sensing cells of Arabidopsis inflorescence stem. Plant Cell Physiol 55:811–822PubMedPubMedCentralCrossRefGoogle Scholar
  40. Herbert TJ, Larsen PB (1985) Leaf movement in Calathea lutea (Marantaceae). Oecologia 67:238–243PubMedCrossRefGoogle Scholar
  41. Hillman WS, Koukkari WL (1967) Phytochrome effects in nyctinastic leaf movements of Albizzia julibrissin and some other legumes. Plant Physiol 42:1413–1418PubMedPubMedCentralCrossRefGoogle Scholar
  42. Huang W, Zhang S-B, Cao K-F (2012) Evidence for leaf fold to remedy the deficiency of physiological photoprotection for photosystem II. Photosynth Res 110:185–191PubMedCrossRefGoogle Scholar
  43. Jurik TW, Zhang HZ, Pleasants JM (1990) Ecophysiological consequences of nonrandom leaf orientation in the prairie compass plant, Silphium laciniatum. Oecologia 82:180–186PubMedCrossRefGoogle Scholar
  44. Kadioglu A, Terzi R (2007) A dehydration avoidance mechanism: leaf rolling. Bot Rev 73:290–302CrossRefGoogle Scholar
  45. Kadioglu A, Terzi R, Saruhan N, Saglam A (2012) Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Sci 182:42–48PubMedCrossRefGoogle Scholar
  46. Kao WY, Forseth IN (1992a) Dirunal leaf movement, chlorophyll fluorescence and carbon assimilation in soybean grown under different nitrogen and water availabilities. Plant Cell Environ 15:703–710CrossRefGoogle Scholar
  47. Kao WY, Forseth IN (1992b) Responses of gas-exchange and phototropic leaf orientation in soybean to soil-water availability, leaf water potential, air-temperature, and photosynthetic photon flux. Environ Exp Bot 32:153–161CrossRefGoogle Scholar
  48. Kao WY, Lin B-L (2010) Phototropic leaf movements and photosynthetic performance in an amphibious fern, Marsilea quadrifolia. J Plant Res 123:645–653PubMedCrossRefGoogle Scholar
  49. Knapp AK, Smith WK (1988) Effect of water-stress on stomatal and photosynthetic responses in subalpine plants to cloud patterns. Am J Bot 75:851–858CrossRefGoogle Scholar
  50. Knapp AK, Smith WK (1990) Contrasting stomatal responses to variable sunlight in 2 sub-alpine herbs. Am J Bot 77:226–231PubMedCrossRefGoogle Scholar
  51. Koller D (1981) Solar tracking (phototropism) in leaves of Lavatera cretica and Malva parviflora. Carnegie Institute of Washington Yearbook 80:72–75Google Scholar
  52. Koller D (1990) Light-driven leaf movements. Plant Cell Environ 13:615–632CrossRefGoogle Scholar
  53. Koller D (2011) The restless plant. Harvard University Press, Cambridge, MAGoogle Scholar
  54. Kutschera U, Niklas KJ (2013) Cell division and turgor-driven stem elongation in juvenile plants: a synthesis. Plant Sci 207:45–56PubMedCrossRefGoogle Scholar
  55. Lebkuecher JG, Eickmeier WG (1993) Physiological benefits of stem curling for resurrection plants in the field. Ecology 74:1073–1080CrossRefGoogle Scholar
  56. Lee Y, Jung J-W, Kim S-K, Hwang Y-S, Lee J-S, Kim S-H (2008) Ethylene-induced opposite redistributions of calcium and auxin are essential components in the development of tomato petiolar epinastic curvature. Plant Physiol Biochem 46:685–693PubMedCrossRefGoogle Scholar
  57. Lockhart JA (1965) An analysis of irreversible plant cell elongation. J Theor Biol 8:264–275PubMedCrossRefPubMedCentralGoogle Scholar
  58. Ludlow MM, Björkman O (1984) Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions: damage by excessive light and heat. Planta 161:505–518PubMedCrossRefPubMedCentralGoogle Scholar
  59. Lüttge U (2003) Circadian rhythmicity: is the “biological clock” hardware or software? Prog Bot 64(64):277–319Google Scholar
  60. Lüttge U, Hertel B (2009) Diurnal and annual rhythms in trees. Trees-Struct Funct 23:683–700CrossRefGoogle Scholar
  61. Mooney HA, Ehleringer JR (1978) The carbon gain benefits of solar tracking in a desert annual. Plant Cell Environ 1:307–311CrossRefGoogle Scholar
  62. Moran N (2007) Rhythmic leaf movements: physiological and molecular aspects of rhythms in plants. In: Mancuso S, Shabala S (eds) Rhythms in plants: phenomenology, mechanisms, and adaptive significance. Springer, Berlin/Heidelberg, pp 3–37CrossRefGoogle Scholar
  63. Moulia B (1994) The biomechanics of leaf rolling. Biomimetics 2:267–281Google Scholar
  64. Moulia B, Coutand C, Lenne C (2006) Posture control and skeletal mechanical acclimation in terrestrial plants: implications for mechanical modeling of plant architecture. Ame J Bot 93:1477–1489CrossRefGoogle Scholar
  65. Nar H, Saglam A, Terzi R, Varkonyi Z, Kadioglu A (2009) Leaf rolling and photosystem II efficiency in Ctenanthe setosa exposed to drought stress. Photosynthetica 47:429–436CrossRefGoogle Scholar
  66. Neufeld HS, Meinzer FC, Wisdom CS, Sharifi MR, Rundel PW, Neufeld MS, Goldring Y, Cunningham GL (1988) Canopy architecture of Larrea tridentata (DC) Coville, a desert shrub – foliage orientation and direct beam radiation interception. Oecologia 75:54–60PubMedCrossRefGoogle Scholar
  67. Neuner G, Braun V, Buchner O, Taschler D (1999) Leaf rosette closure in the alpine rock species Saxifraga paniculata mill.: significance for survival of drought and heat under high irradiation. Plant Cell Environ 22:1539–1548CrossRefGoogle Scholar
  68. Niinemets U, Fleck S (2002) Petiole mechanics, leaf inclination, morphology, and investment in support in relation to light availability in the canopy of Liriodendron tulipifera. Oecologia 132:21–33PubMedCrossRefGoogle Scholar
  69. Nilsen ET (1985) Seasonal and diurnal leaf movements of Rhododendron maximum L. In contrasting irradiance environments. Oecologia 65:296–302PubMedCrossRefGoogle Scholar
  70. Nilsen ET (1986) Quantitative phenology and leaf survivorship of Rhododendron maximum in contrasting irradiance environments of the southern Appalachian Mountains. Am J Bot 73:822–831CrossRefGoogle Scholar
  71. Nilsen ET (1987) Influence of water relations and temperature on leaf movements of Rhododendron species. Plant Physiol 83:607–612PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nilsen ET (1990) Why do Rhododendron leaves curl. Arnoldia 50:30–35Google Scholar
  73. Nilsen ET (1991) The relationship between freezing tolerance and thermotropic leaf movement in 5 Rhododendron species. Oecologia 87:63–71PubMedCrossRefGoogle Scholar
  74. Nilsen ET (1992) Thermonastic leaf movements – a synthesis of research with Rhododendron. Bot J Linnean Soc 110:205–233CrossRefGoogle Scholar
  75. Nilsen ET (1995) Stem photosynthesis: extent, patterns, and role in plant carbon economy. In: Gartner B (ed) Stems and trunks in plant form and function. Academic Press, pp 223–240 San DiegoCrossRefGoogle Scholar
  76. Nilsen ET, Bao Y (1988) The ecophysiological significance of thermotropic leaf movements in Rhododendron maximum. Am J Bot 75:126–126CrossRefGoogle Scholar
  77. Nilsen ET, Sharifi MR (1994) Acclimation of stem photosynthesis to habitat conditions by two legumes in the Sonoran and Mojave deserts of California. Plant Physiol 105:1385–1391PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nilsen ET, Karpa D, Mooney HA, Field CB (1993) Patterns of stem assimilation in two species of invasive legumes in coastal California. Am J Bot 80:1126–1136CrossRefGoogle Scholar
  79. Nilsen ET, Arora R, Upmanyu M (2014) Thermonastic leaf movements in Rhododendron during freeze-thaw events: patterns, functional significances, and causes. Environ Exp Bot 106:34–43CrossRefGoogle Scholar
  80. Nobel PS, Forseth IN, Long SP (1993) Canopy structure and light interception. In: Hall DO, Scurlock JMO, Bolhar-Nordenkampf HR, Leegood RC, Long SP (eds) Photosynthesis and production in a changing environment: a field and laboratory Mannual. Springer, Berlin/Heidelberg, pp 79–90Google Scholar
  81. Noctor G, Lelarge-Trouverie C, Mhamdi A (2015) The metabolomics of oxidative stress. Phytochemistry 112:33–53PubMedCrossRefGoogle Scholar
  82. Okamura M, Hirose T, Hashida Y, Ohsugi R, Aoki N (2015) Suppression of starch synthesis in rice stems splays tiller angle due to gravitropic insensitivity but does not affect yield. Funct Plant Biol 42:31–41CrossRefGoogle Scholar
  83. Pierik R, de Wit M (2014) Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues. J Exp Bot 65:2815–2824PubMedCrossRefGoogle Scholar
  84. Powles SB, Bjorkman O (1981) Leaf movement in the shade species Oxalis oregana 2. Role in protection against injury by intense light. In: Ebert JD (ed) Carnegie Institution of Washington year book, 1980/1981. Carnegie Institution of Washington, Washington, DC, pp 63–66Google Scholar
  85. Prichard JM, Forseth IN (1988a) Photosynthetic responses of 2 heliotropic legumes from contrasting habitats. Plant Cell Environ 11:591–601CrossRefGoogle Scholar
  86. Prichard JM, Forseth IN (1988b) Rapid leaf movement, microclimate, and water relations of 2 temperate legumes in 3 contrasting habitats. Am J Bot 75:1201–1211CrossRefGoogle Scholar
  87. Reich PB (2014) The world-wide ‘fast-slow’ plant economic spectrum: a traits manifesto. J Ecol 102:275–301CrossRefGoogle Scholar
  88. Roden JS (2003) Modeling the light interception and carbon gain of individual fluttering aspen (Populus tremuloides Michx) leaves. Trees-Struct Funct 17:117–126Google Scholar
  89. Roden JS, Pearcy RW (1993) The effect of flutter on the temperature of poplar leaves and its implications for carbon gain. Plant Cell Environ 16:571–577CrossRefGoogle Scholar
  90. Russell RB, Lei TT, Nilsen ET (2009) Freezing induced leaf movements and their potential implications to early spring carbon gain: Rhododendron maximum as exemplar. Funct Ecol 23:463–471CrossRefGoogle Scholar
  91. Sailaja MV, Das VSR (1996) Leaf solar tracking response exhibits diurnal constancy in photosystem II efficiency. Environ Exp Bot 36:431–438CrossRefGoogle Scholar
  92. Satter RL, Galston AW (1981) Mechanisms of control of leaf movements. Annu Rev Plant Physiol Plant Mol Biol 32:83–110CrossRefGoogle Scholar
  93. Scorza LCT, Dornelas MC (2011) Plants on the move: towards common mechanisms governing mechanically induced plant movements. Plant Signal Behav 6:1979–1986PubMedPubMedCentralCrossRefGoogle Scholar
  94. Shell GSG, Lang ARG (1976) Movements of sunflower leaves over a 24-h period. Agric Meteorol 16:161–170CrossRefGoogle Scholar
  95. Simioni G, Durand-Gillmann M, Huc R (2013) Asymmetric competition increases leaf inclination effect on light absorption in mixed canopies. Ann Forest Sci 70:123–131CrossRefGoogle Scholar
  96. Smith WK, Berry ZC (2013) Sunflecks? Tree Physiol 33:233–237PubMedCrossRefGoogle Scholar
  97. Smith WK, Hughes NM (2009) Progress in coupling plant form and photosynthetic function. Castanea 74:1–26CrossRefGoogle Scholar
  98. Soares AS, Driscoll SP, Olmos E, Harbinson J, Arrabaca MC, Foyer CH (2008) Adaxial/abaxial specification in the regulation of photosynthesis and stomatal opening with respect to light orientation and growth with CO2 enrichment in the C4 species Paspalum dilatatum. New Phytol 177:186–198PubMedGoogle Scholar
  99. Stewart JR, Graves WR (2004) Photosynthesis and growth of Carolina buckthorn (Rhamnus caroliniana) during drought and flooding: comparisons to the invasive common buckthorn (Rhamnus cathartica). Acta Hortic (630):143–146Google Scholar
  100. Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant-insect interactions under bacterial influence: ecological implications and underlying implications. J Exp Bot 66:467–478PubMedCrossRefGoogle Scholar
  101. Telewski FW (2012) Is windswept tree growth negative thigmotropism? Plant Sci 184:20–28PubMedCrossRefGoogle Scholar
  102. Ueda M, Nakamura Y (2007) Chemical basis of plant leaf movement. Plant Cell Physiol 48:900–907PubMedCrossRefGoogle Scholar
  103. van Zanten M, Pons TL, Janssen JAM, Voesenek LACJ, Peeters AJM (2010) On the relevance and control of leaf angle. Crit Rev Plant Sci 29:300–316CrossRefGoogle Scholar
  104. Vandenbrink JP, Brown EA, Harmer SL, Blackman BK (2014) Turning heads: the biology of solar tracking in sunflower. Plant Sci 224:20–26PubMedCrossRefGoogle Scholar
  105. Verhoeven AS (2013) Recovery kinetics of photochemical efficiency in winter stressed conifers: the effects of growth light environment, extent of the season and species. Physiol Plant 147:147–158PubMedCrossRefGoogle Scholar
  106. Verhoeven AS (2014) Sustained energy dissipation in winter evergreens. New Phytol 201:57–65CrossRefGoogle Scholar
  107. Verhoeven AS, Adams WW III, Demmig-Adams B (1999) The xanthophyll cycle and acclimation ofPinus ponderosa and Malva neglecta to winter stress. Oecologia 118:277–287PubMedCrossRefPubMedCentralGoogle Scholar
  108. Verhoeven AS, Swanberg A, Thao M, Whiteman J (2005) Seasonal changes in leaf antioxidant systems and xanthophyll cycle characteristics in Taxus x media growing in sun and shade environments. Physiol Plant 123:428–434CrossRefGoogle Scholar
  109. Werk KS, Ehleringer J (1985) Photosynthetic characteristics of Lactuca serriola L. Plant Cell Environ 8:345–350CrossRefGoogle Scholar
  110. Young DR, Smith WK (1979) Influence of sunflecks on the temperature and water relations of 2 subalpine understory congeners. Oecologia 43:195–205PubMedCrossRefGoogle Scholar
  111. Zhang Y-L, Zhang H-Z, Du M-W, Li W, Luo H-H, Chow W-S, Zhang W-F (2010) Leaf wilting movement can protect water-stressed cotton (Gossypium hirsutum L.) plants against photoinhibition of photosynthesis and maintain carbon assimilation in the field. J Plant Biol 53:52–60CrossRefGoogle Scholar
  112. Zhang Y-L, Hu YY, Luo HH, Chow WS, Zhang WF (2011) Two distinct strategies of cotton and soybean differing in leaf movement to perform photosynthesis under drought in the field. Funct Plant Biol 38:567–575CrossRefGoogle Scholar
  113. Zhu CG, Chen YN, Li WH, Chen XL, He GZ (2015) Heliotropic leaf movement of Sophora alopecuroides L.: an efficient strategy to optimise photochemical performance. Photosynthetica 53:231–240CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesVirginia TechBlacksburgUSA
  2. 2.Biology/Integrative Organismal SystemsNational Science FoundationArlingtonUSA

Personalised recommendations