Abstract
Fluxes of carbon and water along a vertical profile within a canopy, particularly the associations between canopy and ecosystem levels, are not well studied. In this study, gas exchange along the vertical profile in a maize canopy was examined. The relationships between leaf- and ecosystem-level carbon and water fluxes were compared. The results from research conducted over two growing seasons showed that during vegetative growth, the top and middle leaf layers in the canopy contribute most to the carbon and water fluxes of the entire canopy. During the grain-filling stage, gas exchange processes were performed mostly in the middle leaves with and near the ears. Significant relationships were observed between the net ecosystem CO2 exchange rate (NEE) plus soil respiration and the assumed canopy levels (Acanopy) and between evapotranspiration rates at the ecosystem (ET) and assumed canopy levels (Ecanopy). This highlights the close associations between these parameters by integrating the leaf gas exchange rates measured in a conventional leaf cuvette and those at the ecosystem level via the eddy covariance technique. These results improve our understanding of how carbon assimilation varies vertically within a canopy, highlighting the critical role of ear leaves.
Similar content being viewed by others
References
Allison JCS, Watson DJ (1966) The production and distribution of dry matter in maize after flowering. Ann Bot 30:365–381. https://doi.org/10.1093/oxfordjournals.aob.a084082
Bachofen C, D’Odorico P, Buchmann N (2020) Light and VPD gradients drive foliar nitrogen partitioning and photosynthesis in the canopy of European beech and silver fir. Oecologia 192:323–339. https://doi.org/10.1007/s00442-019-04583-x
Baldocchi DD (2020) How eddy covariance flux measurements have contributed to our understanding of global change biology. Glob Change Biol 26:242–260. https://doi.org/10.1111/gcb.14807
Baldocchi DD, Hicks BB, Meyers TP (1988) Measuring biosphere–atmosphere exchanges of biologically related gases with micrometeorological methods. Ecology 69:1331–1340. https://doi.org/10.2307/1941631
Baldocchi DD (2003) Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Glob Change Biol 9:479–492. https://doi.org/10.1046/j.1365-2486.2003.00629.x
Barron-Gafford GA, Scott RL, Jenerette GD, Hamerlynck EP, Huxman TE (2013) Landscape and environmental controls over leaf and ecosystem carbon dioxide fluxes under woody plant expansion. J Ecol 101:1471–1483. https://doi.org/10.1111/1365-2745.12161
Bonelli LE, Andrade FH (2020) Maize radiation use-efficiency response to optimally distributed foliar-nitrogen-content depends on canopy leaf-area index. Field Crops Res 247:107557. https://doi.org/10.1016/j.fcr.2019.107557
Brouwer B, Ziolkowska A, Bagard M, Keech O, Gardeström P (2012) The impact of light intensity on shade-induced leaf senescence. Plant Cell Environ 35:1084–1098. https://doi.org/10.1111/j.1365-3040.2011.02474.x
Carmo-Silva E, Andralojc PJ, Scales JC, Driever SM, Mead A, Lawson T, Raines CA, Parry MA (2017) Phenotyping of field-grown wheat in the UK highlights contribution of light response of photosynthesis and flag leaf longevity to grain yield. J Exp Bot 68:3473–3486. https://doi.org/10.1093/jxb/erx169
Chen Y, Wu D, Mu X, Xiao C, Chen F, Yuan L, Mi G (2016) Vertical distribution of photosynthetic nitrogen use efficiency and its response to nitrogen in field-grown maize. Crop Sci 56:397–407. https://doi.org/10.2135/cropsci2015.03.0170
Chen T-W, Stützel H, Kahlen K (2018) High light aggravates functional limitations of cucumber canopy photosynthesis under salinity. Ann Bot 121:797–807. https://doi.org/10.1093/aob/mcx100
Cleary MB, Naithani KJ, Ewers BE, Pendall E (2015) Upscaling CO2 fluxes using leaf, soil and chamber measurements across successional growth stages in a sagebrush steppe ecosystem. J Arid Environ 121:43–51. https://doi.org/10.1016/j.jaridenv.2015.05.013
Collison RF, Raven EC, Pignon CP, Long SP (2020) Light, not age, underlies the maladaptation of maize and miscanthus photosynthesis to self-shading. Front Plant Sci 11:783. https://doi.org/10.3389/fpls.2020.00783
Cushman KC, Kellner JR (2019) Prediction of forest aboveground net primary production from high-resolution vertical leaf-area profiles. Ecol Lett 22:538–546. https://doi.org/10.1111/ele.13214
Edmeades GO, Daynard TB (1979) The relationship between final yield and photosynthesis at flowering in individual maize plants. Can J Plant Sci 59:585–601. https://doi.org/10.4141/cjps79-097
Escobar-Gutiérrez AJ, Combe L (2012) Senescence in field-grown maize: from flowering to harvest. Field Crops Res 134:47–58. https://doi.org/10.1016/j.fcr.2012.04.013
Evers JB, Letort V, Renton M, Kang M (2018) Computational botany: advancing plant science through functional–structural plant modelling. Ann Bot 121:767–772. https://doi.org/10.1093/aob/mcy050
Francis CA, Rutger JN, Palmer AFE (1969) A rapid method for plant leaf area estimation in maize (Zea mays L.). Crop Sci 9:537–539. https://doi.org/10.2135/cropsci1969.0011183X000900050005x
Gu J, Yin X, Stomph TJ, Struik PC (2014) Can exploiting natural genetic variation in leaf photosynthesis contribute to increasing rice productivity? A simulation analysis. Plant Cell Environ 37:22–34
Han GX, Zhou GS, Xu ZZ, Yang Y, Liu JL, Shi KQ (2007) Soil temperature and biotic factors drive the seasonal variation of soil respiration in a maize (Zea mays L.) agricultural ecosystem. Plant Soil 2911:5–26. https://doi.org/10.1007/s11104-006-9170-8
Hanway JJ (1971) How a corn plant develops. Iowa Coop Ext Servo Spec Rep 48:18
Hayek MN, Wehr R, Longo M, Hutyra LR, Wiedemann K, Munger JW, Bonal D, Saleska SR, Fitzjarrald DR, Wofsy SC (2018) A novel correction for biases in forest eddy covariance carbon balance. Agric For Meteorol 250:90–101. https://doi.org/10.1016/j.agrformet.2017.12.186
Hikosaka K, Anten NP, Borjigidai A, Kamiyama C, Sakai H, Hasegawa T, Oikawa S, Iio A, Watanabe M, Koike T, Nishina K (2016a) A meta-analysis of leaf nitrogen distribution within plant canopies. Ann Bot 118:239–247. https://doi.org/10.1093/aob/mcw099
Hikosaka K, Kumagai TO, Ito A (2016b) Modeling canopy photosynthesis. Canopy photosynthesis: from basics to applications. Springer, Netherlands, pp 239–268
Hirose T (2005) Development of the Monsi-Saeki theory on canopy structure and function. Ann Bot 95:483–494. https://doi.org/10.1093/aob/mci047
Hussain MZ, Vanloocke A, Siebers MH, Ruiz-Vera UM, Cody Markelz RJ, Leakey AD, Ort DR, Bernacchi CJ (2013) Future carbon dioxide concentration decreases canopy evapotranspiration and soil water depletion by field-grown maize. Glob Chang Biol 19:1572–1584. https://doi.org/10.1111/gcb.12155
Jans WW, Jacobs CM, Kruijt B, Elbers A, Barendse S, Moors EJ (2010) Carbon exchange of a maize (Zea mays L.) crop: Influence of phenology. Agr Ecosyst Environ 139:316–324. https://doi.org/10.1016/j.agee.2010.06.008
Kim SH, Sicher RC, Bae H, Gitz DC, Baker J, Timlin DJ, Reddy VR (2006) Canopy photosynthesis, evapotranspiration, leaf nitrogen, and transcription profiles of maize in response to CO2 enrichment. Glob Change Biol 12:588–600. https://doi.org/10.1111/j.1365-2486.2006.01110.x
Li YB, Song H, Zhou L, Xu ZZ, Zhou GS (2019a) Vertical distributions of chlorophyll and nitrogen and their associations with photosynthesis under drought and rewatering regimes in a maize field. Agric For Meteorol 272–273:40–54. https://doi.org/10.1016/j.agrformet.2019.03.026
Li YJ, Zhou L, Xu ZZ, Zhou GS (2009) Comparison of water vapour, heat and energy exchanges over agricultural and wetland ecosystems. Hydrol Process 23:2069–2080. https://doi.org/10.1002/hyp.7339
Li X, Gentine P, Lin C, Zhou S, Sun Z, Zheng Y, Liu J, Zheng C (2019b) A simple and objective method to partition evapotranspiration into transpiration and evaporation at eddy-covariance sites. Agric For Meteorol 265:171–182. https://doi.org/10.1016/j.agrformet.2018.11.017
Liu G, Hou P, Xie R, Ming B, Wang K, Liu W, Yang Y, Xu W, Chen J, Li S (2019) Nitrogen uptake and response to radiation distribution in the canopy of high-yield maize. Crop Sci 59:1236–1247. https://doi.org/10.2135/cropsci2018.09.0567
Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401. https://doi.org/10.1093/jxb/erg262
Luetchens J, Lorenz AJ (2018) Changes in dynamic leaf traits in maize associated with year of hybrid release. Crop Sci 58:551–563. https://doi.org/10.2135/cropsci2017.04.0256
Ma SY, Osuna JL, Verfaillie J, Baldocchi DD (2017) Photosynthetic responses to temperature across leaf–canopy–ecosystem scales: a 15-year study in a Californian oak-grass savanna. Photosynth Res 132:277–291. https://doi.org/10.1007/s11120-017-0388-5
Minchin PEH, Lacointe A (2005) New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol 166:771–779. https://doi.org/10.1111/j.1469-8137.2005.01323.x
Muchow RC, Sinclair TR (1994) Nitrogen response of leaf photosynthesis and canopy radiation use efficiency in field-grown maize and sorghum. Crop Sci 34:721–727. https://doi.org/10.2135/cropsci1994.0011183X003400030022x
Murchie EH, Kefauver S, Araus JL, Muller O, Rascher U, Flood PJ, Lawson T (2018) Measuring the dynamic photosynthome. Ann Bot 122:207–220. https://doi.org/10.1093/aob/mcy087
Parvin S, Uddin S, Tausz-Posch S, Armstrong R, Tausz M (2020) Carbon sink strength of nodules but not other organs modulates photosynthesis of faba bean (Vicia faba L.) grown under elevated [CO2] and different water supply. New Phytol. https://doi.org/10.1111/nph.16520
Peng Y, Li C, Fritschi FB (2014) Diurnal dynamics of maize leaf photosynthesis and carbohydrate concentrations in response to differential N availability. Environ Exp Bot 99:18–27. https://doi.org/10.1016/j.envexpbot.2013.10.013
NBS (2020) National Data from National Bureau of Statistics of China. http://data.stats.gov.cn/english/easyquery.htm?cn=C01. Accessed 30 Mar 2020
Qi HY, Zhou GS, Xu ZZ (2008) Vertical distribution characteristics of photosynthetically active radiation in maize canopy and its controlling factors. J Meteorol Environ 24:22–26
Ordóñez RA, Savin R, Cossani CM, Slafer GA (2018) Maize grain weight sensitivity to source–sink manipulations under a wide range of field conditions. Crop Sci 58:2542–2557. https://doi.org/10.2135/cropsci2017.11.0676
Pattey E, Rochette P, Desjardins RL, Dube PA (1991) Estimation of the net CO2 assimilation rate of a maize (Zea mays L.) canopy from leaf chamber measurements. Agric For Meteorol 55:37–57. https://doi.org/10.1016/0168-1923(91)90021-H
Restrepo-Coupe N, Huete A, Davies K, Cleverly J, Beringer J, Eamus D, van Gorsel E, Hutley LB, Meyer WS (2016) MODIS vegetation products as proxies of photosynthetic potential along a gradient of meteorologically and biologically driven ecosystem productivity. Biogeosci 13:5587–5608. https://doi.org/10.5194/bgd-12-19213-2015
Ritchie SW, Hanway JJ, Benson GO, Herman JC (1993) How a corn plant develops. Special Report No. 48. Ames, IA (USA), Iowa State University
Sadras VO, Echarte L, Andrade FH (2000) Profiles of leaf senescence during reproductive growth of sunflower and maize. Ann Bot 85:187–195. https://doi.org/10.1006/anbo.1999.1013
Sanchez-Bragado R, Vicente R, Molero G, Serret MD, Maydup ML, Araus JL (2020) New avenues for increasing yield and stability in C3 cereals: exploring ear photosynthesis. Curr Opin Plant Biol. https://doi.org/10.1016/j.pbi.2020.01.001
Silva LC, Lambers H (2020) Soil-plant-atmosphere interactions: structure, function, and predictive scaling for climate change mitigation. Plant Soil. https://doi.org/10.1007/s11104-020-04427-1
Smith NG, Dukes JS (2018) Drivers of leaf carbon exchange capacity across biomes at the continental scale. Ecology 99:1610–1620. https://doi.org/10.1002/ecy.2370
Soegaard H, Jensen NO, Boegh E, Hasager CB, Schelde K, Thomsen A (2003) Carbon dioxide exchange over agricultural landscape using eddy correlation and footprint modelling. Agric For Meteorol 114:53–173. https://doi.org/10.1016/S0168-1923(02)00177-6
Song H, Li YB, Zhou L, Xu ZZ, Zhou GS (2018) Maize leaf functional responses to drought episode and rewatering. Agric For Meteorol 249:57–70. https://doi.org/10.1016/j.agrformet.2017.11.023
Song Q, Chen D, Long SP, Zhu XG (2017) A user-friendly means to scale from the biochemistry of photosynthesis to whole crop canopies and production in time and space-development of Java WIMOVAC. Plant Cell Environ 40:51–55. https://doi.org/10.1111/pce.12816
Song Q, Xiao H, Xiao X, Zhu XG (2016) A new canopy photosynthesis and transpiration measurement system (CAPTS) for canopy gas exchange research. Agric For Meteorol 217:101–107. https://doi.org/10.1016/j.agrformet.2015.11.020
Steduto P, Hsiao TC (1998) Maize canopies under two soil water regimes: II. Seasonal trends of evapotranspiration, carbon dioxide assimilation and canopy conductance, and as related to leaf area index. Agric For Meteorol 89:185–200. https://doi.org/10.1016/S0168-1923(97)00084-1
Stirling CM, Aguilera C, Baker NR, Long SP (1994) Changes in the photosynthetic light response curve during leaf development of field grown maize with implication for modelling canopy photosynthesis. Photosynth Res 42:217–225. https://doi.org/10.1007/BF00018264
Tamhane AC (1977) Multiple comparisons in model I one-way ANOVA with unequal variances. Commun Stat Theor Meth 6:15–32. https://doi.org/10.1080/03610927708827466
Timlin DJ, Naidu TCM, Fleisher DH, Reddy VR (2017) Quantitative effects of phosphorus on maize canopy photosynthesis and biomass. Crop Sci 57:3156–3169. https://doi.org/10.2135/cropsci2016.11.0970
Ubierna N, Cernusak LA (2019) Preface: advances in modelling photosynthetic processes in terrestrial plants. Photosynth Res 141:1–3. https://doi.org/10.1007/s11120-019-00651-8
Urban O, Klem K, Havránková K, Holišová P, Navratil M et al (2012) Impact of clear and cloudy sky conditions on the vertical distribution of photosynthetic CO2 uptake within a spruce canopy. Funct Ecol 26:46–55. https://doi.org/10.1111/j.1365-2435.2011.01934.x
Valayamkunnath P, Sridhar V, Zhao W, Allen RG (2018) Intercomparison of surface energy fluxes, soil moisture, and evapotranspiration from eddy covariance, large-aperture scintillometer, and modeling across three ecosystems in a semiarid climate. Agric For Meteorol 248:22–47. https://doi.org/10.1016/j.agrformet.2017.08.025
Valentinuz OR, Tollenaar M (2004) Vertical profile of leaf senescence during the grain-filling period in older and newer maize hybrids. Crop Sci 44:827–834. https://doi.org/10.2135/cropsci2004.8270
Vitale L, Di Tommasi P, D’Urso G, Magliulo V (2016) The response of ecosystem carbon fluxes to LAI and environmental drivers in a maize crop grown in two contrasting seasons. Int J Biometeorol 60:411–420. https://doi.org/10.1007/s00484-015-1038-2
Wagle P, Gowda PH, Xiao X, Anup KC (2016) Parameterizing ecosystem light use efficiency and water use efficiency to estimate maize gross primary production and evapotranspiration using MODIS EVI. Agric For Meteorol 222:87–97. https://doi.org/10.1016/j.agrformet.2016.03.009
Wang YL, Zhou GS, Wang YH (2008) Environmental effects on net ecosystem CO2 exchange at half-hour and month scales over Stipa krylovii steppe in northern China. Agric For Meteorol 148:714–722. https://doi.org/10.1016/j.agrformet.2008.01.013
Wang H, Jia G, Zhang A, Miao C (2016) Assessment of spatial representativeness of eddy covariance flux data from flux tower to regional grid. Remote Sens 8(9):742. https://doi.org/10.3390/rs8090742
Webb EK, Pearman GI, Leuning R (1980) Correction of flux measurements for density effects due to heat and water vapour transfer. Q J Roy Meteorol Soc 106:85–100. https://doi.org/10.1002/qj.49710644707
Wofsy SC, Goulden ML, Munger JW, Fan SM, Bakwin PS, Daube BC, Bassow SL, Bazzaz FA (1993) Net exchange of CO2 in a mid-latitude forest. Science 260:1314–1317. https://doi.org/10.1126/science.260.5112.1314
Xu ZZ, Zhou GS, Han GX, Li YJ (2011) Photosynthetic potential and its association with lipid peroxidation in response to high temperature at different leaf ages in maize. J Plant Growth Regul 30:41–50. https://doi.org/10.1007/s00344-010-9167-7
Xu ZZ, Zhou GS, Wang YL, Han GX, Li YJ (2008) Changes in chlorophyll fluorescence in maize plants with imposed rapid dehydration at different leaf ages. J Plant Growth Regul 27:83–92. https://doi.org/10.1007/s00344-007-9035-2
Xu ZZ, Zhou GS, Han GX, Li YJ (2018) The relationship between leaf and ecosystem CO2 exchanges in a maize field. Acta Physiol Plant 40:156. https://doi.org/10.1007/s11738-018-2732-6
Yang X, Tang J, Mustard JF, Wu J, Zhao K, Serbin S, Lee JE (2016) Seasonal variability of multiple leaf traits captured by leaf spectroscopy at two temperate deciduous forests. Remote Sens Environ 179:1–12. https://doi.org/10.1016/j.rse.2016.03.026
Yuan W, Liu S, Zhou G, Zhou G, Tieszen LL, Baldocchi D, Bernhofer C, Gholz H, Goldstein AH, Goulden ML, Hollinger DY (2007) Deriving a light use efficiency model from eddy covariance flux data for predicting daily gross primary production across biomes. Agric For Meteorol 143:189–207. https://doi.org/10.1016/j.agrformet.2006.12.001
Zhao J, Yang X, Lin X, Sassenrath GF, Dai S, Lv S, Chen X, Chen F, Mi G (2015) Radiation interception and use efficiency contributes to higher yields of newer maize hybrids in Northeast China. Agron J 107:473–1480. https://doi.org/10.2134/agronj14.0510
Zhao K, Dong B, Jia Z, Ma L (2018) Effect of climatic factors on the temporal variation of stem respiration in Larix principis-rupprechtii Mayr. Agric For Meteorol 248:441–448. https://doi.org/10.1016/j.agrformet.2017.10.033
Zhu XG, Song Q, Ort DR (2012) Elements of a dynamic systems model of canopy photosynthesis. Curr Opin Plant Biol 15:237–244. https://doi.org/10.1016/j.pbi.2012.01.010
Acknowledgements
We are grateful to Chunqiao Shi, Hongyan Qi, Tao Liang, Yang Yang, and Jingli Liu for their great help during this study.
Funding
The study was funded by National Key Research and Development Program of China (2016YFD0300106), and China Special Fund for Meteorological Research in the Public Interest (GYHY201506001-3).
Author information
Authors and Affiliations
Contributions
ZX and GZ conceived and designed the study. ZX and QH analyzed the data and wrote the draft manuscript. The three authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the Supplementary Information.
Rights and permissions
About this article
Cite this article
Xu, Z., Zhou, G. & He, Q. Vertical distribution of gas exchanges and their integration throughout the entire canopy in a maize field. Photosynth Res 147, 269–281 (2021). https://doi.org/10.1007/s11120-020-00817-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-020-00817-9