Abstract
Leaf anatomy and the stomatal development of developing leaves of plants have been shown to be regulated by the same light environment as that of mature leaves, but no report has yet been written on whether such a long-distance signal from mature leaves regulates the total leaf area of newly emerged leaves. To explore this question, we created an investigation in which we collected data on the leaf area, leaf mass per area (LMA), leaf anatomy, cell size, cell number, gas exchange and soluble sugar content of leaves from three soybean varieties grown under full sunlight (NS), shaded mature leaves (MS) or whole plants grown in shade (WS). Our results show that MS or WS cause a marked decline both in leaf area and LMA in newly developing leaves. Leaf anatomy also showed characteristics of shade leaves with decreased leaf thickness, palisade tissue thickness, sponge tissue thickness, cell size and cell numbers. In addition, in the MS and WS treatments, newly developed leaves exhibited lower net photosynthetic rate (Pn), stomatal conductance (Gs) and transpiration rate (E), but higher carbon dioxide (CO2) concentration in the intercellular space (Ci) than plants grown in full sunlight. Moreover, soluble sugar content was significantly decreased in newly developed leaves in MS and WS treatments. These results clearly indicate that (1) leaf area, leaf anatomical structure, and photosynthetic function of newly developing leaves are regulated by a systemic irradiance signal from mature leaves; (2) decreased cell size and cell number are the major cause of smaller and thinner leaves in shade; and (3) sugars could possibly act as candidate signal substances to regulate leaf area systemically.
Similar content being viewed by others
References
Araya T, Noguchi KO, Terashima I (2008) Manipulation of light and CO2 environments of the primary leaves of bean (Phaseolus vulgaris L.) affects photosynthesis in both the primary and the first trifoliate leaves: involvement of systemic regulation. Plant Cell Environ 31:50–61
Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology I. Encyclopedia of plant physiology (new series), vol 12/A. Springer, Berlin, pp 57–107
Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2006) Systemic signalling of environmental cues in Arabidopsis leaves. J Exp Bot 57:329–341
Fan XX, Xu ZG, Liu XY, Tang CM, Wang LW, Han XL (2013) Effects of light intensity on the growth and leaf development of young tomato plants grown under a combination of red and blue light. Sci Hort 153:50–55
Francis CA (1989) Biological efficiencies in multiple-cropping system. Adv Agron 42:1–42
Gong W, Qi P, Du J, Sun X, Wu X, Song C, Liu W, Wu Y, Yu X, Yong T (2014) Transcriptome analysis of shade-induced inhibition on leaf size in relay intercropped soybean. Plos One 9:e98465
Gong WZ, Jiang CD, Wu YS, Chen HH, Liu WY, Yang WY (2015) Tolerance vs. avoidance: two strategies of soybean (Glycine max) seedlings in response to shade in intercropping. Photosynthetica 53:259–268
Guo Z, Wang F, Xiang X, Ahammed GJ, Wang M, Onac E, Zhou J, Xia X, Shi K, Yin X, Chen K, Yu J, Foyer CH, Zhou Y (2016) Systemic induction of photosynthesis via illumination of the shoot apex is mediated sequentially by phytochrome B, auxin and hydrogen peroxide in tomato. Plant Physiol 172:1259–1272
Hanson J, Johannesson H, Engstrom P (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol Biol 45:247–262
Jiang CD, Wang X, Gao HY, Shi L, Chow WS (2011) Systemic regulation of leaf anatomical structure, photosynthetic performance, and high-light tolerance in sorghum. Plant Physiol 155:1416–1424
Kim GT, Yano S, Kozuka T, Tsukaya H (2005) Photomorphogenesis of leaves: shade-avoidance and differentiation of sun and shade leaves. Photochem Photobiol Sci 4:770–774
Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246
Koch KE, Ying Z, Wu Y, Avigne WT (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51:417–427
Kozuka T, Horiguchi G, Kim G-T, Ohgishi M, Sakai T, Tsukaya H (2005) The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar. Plant Cell Physiol 46:213–223
Lake J, Quick W, Beerling D, Woodward F (2001) Plant development: signals from mature to new leaves. Nature 411:154–154
Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193
Li T, Liu Y, Shi L, Jiang C (2015) Systemic regulation of photosynthetic function in field-grown sorghum. Plant Physiol Biochem 94:86–94
Lin M-J, Hsu B-D (2004) Photosynthetic plasticity of Phalaenopsis in response to different light environments. J Plant Physiol 161:1259–1268
Liu W, Deng Y, Hussain S, Zou J, Yuan J, Luo L, Yang C, Yuan X, Yang W (2016) Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean [Glycine max (L.) Merr.]. Field Crops Res 196:261–267
Loach K (1967) Shade tolerance in tree seedlings. New Phytol 66:607–621
Luo F-L, Nagel KA, Zeng B, Schurr U, Matsubara S (2009) Photosynthetic acclimation is important for post-submergence recovery of photosynthesis and growth in two riparian species. Ann Bot Lond 104:1435–1444
Luo F-L, Nagel KA, Scharr H, Zeng B, Schurr U, Matsubara S (2011) Recovery dynamics of growth, photosynthesis and carbohydrate accumulation after de-submergence: a comparison between two wetland plants showing escape and quiescence strategies. Ann Bot Lond 107:49–63
Maness N (2010) Extraction and analysis of soluble carbohydrates. In: Sunkar R (ed) Plant stress tolerance: methods and protocols. Humana Press, Totowa, pp 341–370
Matsuda R, Murakami K (2016) Light- and CO2-dependent systemic regulation of photosynthesis. In: Lüttge U, Cánovas FM, Matyssek R (eds) Progress in botany, vol 77. Springer International Publishing, Cham, pp 151–166
Mishio M, Kawakubo N (2015) Variations in leaf morpho-anatomy and photosynthetic traits between sun and shade populations of Eurya japonica (Pentaphylacaceae) whose seeds are dispersed by birds across habitats. Plant Species Biol 30:147–158
Miyazawa S, Livingston NJ, Turpin DH (2006) Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa × P. deltoides). J Exp Bot 57:373–380
Murakami K, Matsuda R, Fujiwara K (2014) Light-induced systemic regulation of photosynthesis in primary and trifoliate leaves of Phaseolus vulgaris: effects of photosynthetic photon flux density (PPFD) versus spectrum. Plant Biol 16:16–21
Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. J Exp Bot 56:449–460
Osmond B, Förster B (2006) Photoinhibition: then and now. In: Demmig-Adams B, Adams WW, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, Dordrecht, pp 11–22
Pearcy RW, Sims DA (1994) Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. In: Caldwell MM, Pearcy RW (eds) Ecophysiological processes above—and belowground, exploitation of environmental heterogeneity by plants. Academic Press, San Diego, pp 145–174
Pons TL, Pearcy RW (1994) Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants. Physiol Plant 92:636–644
Schmitz J, Heinrichs L, Scossa F, Fernie AR, Oelze M-L, Dietz K-J, Rothbart M, Grimm B, Flügge U-I, Häusler RE (2014) The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities. J Exp Bot 65:eru027
Schoch P, Zinsou C, Sibi M (1980) Dependence of the stomatal index on environmental factors during stomatal differentiation in leaves of Vigna sinensis L. 1. Effect of light intensity. J Exp Bot 31:1211–1216
Terashima I, Inoue Y (1985) Palisade tissue chloroplasts and spongy tissue chloroplasts in spinach: biochemical and ultrastructural differences. Plant Cell Physiol 26:63–75
Terashima I, Miyazawa S-I, Hanba YT (2001) Why are sun leaves thicker than shade leaves?—Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105
Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354
Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116
Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New Phytol 161:193–198
Tognetti JA, Pontis HG, Martinez-Noel GM (2013) Sucrose signaling in plants: a world yet to be explored. Plant Signal Behav 8:e23316
Tsukaya H (2002) The leaf index: heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant Cell Physiol 43:372–378
Wind JJ, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614
Wu YS, Gong WZ, Yang F, Wang XC, Yong TW, Yang WY (2015a) Responses to shade and subsequent recovery of soya bean in maize–soya bean relay strip intercropping. Plant Prod Sci 19:206–214
Wu YS, Gong WZ, Liao DP, Wu XL, Yang F, Liu WG, Yong TW, Yang WY (2015b) Effect of shade and light recovery on soybean cultivars (Lines) and its relationship with yield in relay strip intercropping system. Acta Agron Sinica 44:1740–1747
Wu YS, Yang F, Gong WZ, Ahmed S, Fan YF, Wu XL, Yong TW, Liu WG, Shu K, Liu J, Du JB, Yang WY (2017a) Shade adaptive response and yield analysis of different soybean genotypes in relay intercropping systems. J Integr Agric 16:1331–1340
Wu YS, Gong WZ, Yang WY (2017b) Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean. Sci Rep 7:9259
Yang F, Liao DP, Wu XL, Gao RC, Fan YF, Raza MA, Wang XC, Yong TW, Liu WG, Liu J (2017) Effect of aboveground and belowground interactions on the intercrop yields in maize–soybean relay intercropping systems. Field Crops Res 203:16–23
Yano S, Terashima I (2001) Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in chenopodium album. Plant Cell Physiol 42:1303–1310
Yano S, Terashima I (2004) Developmental process of sun and shade leaves in Chenopodium album L. Plant Cell Environ 27:781–793
Acknowledgements
We thank teachers in our team for fruitful discussions and suggestions, and thank Tayan Liang for improving the quality of English of this manuscript, we would also like to thank those who helped improve this manuscript. This research was supported by National Natural Science Foundation of China (nos. 31571615 and 31701371).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wu, Y., Gong, W., Wang, Y. et al. Leaf area and photosynthesis of newly emerged trifoliolate leaves are regulated by mature leaves in soybean. J Plant Res 131, 671–680 (2018). https://doi.org/10.1007/s10265-018-1027-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-018-1027-8