Determination of maximum electron transport rate and its impact on allocation of electron flow

doi:10.17521/cjpe.2017.0320

Abstract

Abstract:

Aims The non-rectangular hyperbolic model (termed as model I) is the main submodel of the FvCB biochemical model, which is used to estimate the maximum electron transport rate (J_max) of plant leaves. The submodel is widely applied to fit the light-response curves of electron transport rate (J-I curves), and obtain J_max. However, it has not been strictly verified whether J_max calculated by model I is consistent with the measured values.

Methods Light-response curves of electron transport rate and of photosynthesis rate of soybean (Glycine max) (under shading and full sunlight) were simultaneously measured by LI-6400-40, then these data were simulated by model I and the mechanistic model of light-response of electron transport rate (termed as model II).

Important findings The results showed that there was the significant differences between J_max estimated by model I and the observation data irrespective of shading and full sunny leaves of soybean. However, there was no significant difference between J_max calculated by model II and the measured value. Because J_max was overestimated by model I, it must lead to overestimate the amount of photosynthetic electron flow to allocate to photorespiration pathway, and magnify the photoprotection of photorespiration on plants. On the contrary, the J_max and saturation light intensity (PAR_sat) obtained by the model II were in very close agreement with the observations. It can be concluded that the model II was superior to the model I in estimates of J_max and PAR_sat. Therefore, we recommend model II to be used as an operational model for fitting J-I curves and accurately assess the role of photorespiration on plant photo-protection.

http://jtp.cnki.net/bilingual/detail/html/ZWSB201804009

Key words: Glycine max, non-rectangular hyperbolic model, mechanistic model, FvCB biochemical model, electron transport rate

Zi-Piao YE, Shi-Hua DUAN, Ting AN, Hua-Jing KANG. Determination of maximum electron transport rate and its impact on allocation of electron flow[J]. Chin J Plant Ecol, 2018, 42(4): 498-507.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2017.0320

https://www.plant-ecology.com/EN/Y2018/V42/I4/498

Figures/Tables 5

References 52

1	Baker NR ( 2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89-113. DOI URL PMID
2	Bellucco V, Marras S, Grimmond CSB, J?rvi L, Sirca C, Spano D ( 2017). Modelling the biogenic CO₂ exchange in urban and non-urban ecosystems through the assessment of light-response curve parameters. Agricultural and Forest Meteorology, 236, 113-122. DOI URL
3	Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ ( 2011). Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnology and Oceanography, 56, 927-938. DOI URL
4	Buckley TN, Diaz-Espejo A ( 2015). Reporting estimates of maximum potential electron transport rate. New Phytologist, 205, 14-17. DOI URL PMID
5	Calama R, Puértolas J, Madrigal G, Pardos M ( 2013). Modeling the environmental response of leaf net photosynthesis in Pinus pinea L. natural regeneration. Ecological Modelling, 251, 9-21. DOI URL
6	Cheng LL, Fuchigami LH, Breen PJ ( 2001). The relationship between photosystem II efficiency and quantum yield for CO₂ assimilation is not affected by nitrogen content in apple leaves. Journal of Experimental Botany, 52, 1865-1872. DOI URL
7	Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM ( 2005). Plasticity in light reactions of photosynthesis for energy production and photoprotection. Journal of Experimental Botany, 56, 395-406. DOI URL PMID
8	dos Santos JUM, de Carvalho GJF, Fearnside PM ( 2013). Measuring the impact of flooding on Amazonian trees: Photosynthetic response models for ten species flooded by hydroelectric dams. Trees, 27, 193-210. DOI URL
9	Dubois JJB, Fiscus EL, Booker FL, Flowers MD, Reid CD ( 2007). Optimizing the statistical estimation of the parameters of the Farquhar-von Caemmerer-Berry model of photosynthesis. New Phytologist, 176, 402-414. DOI URL PMID
10	Epron D, Godard D, Cornic G, Genty B ( 1995). Limitation of net CO₂ assimilation rate by internal resistances to CO₂ transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant,Cell & Environment, 18, 43-51. DOI URL
11	Farquhar GD, Busch FA ( 2017). Changes in the chloroplastic CO₂ concentration explain much of the observed Kok effect: A model. New Phytologist, 214, 570-584. DOI URL PMID
12	Farquhar GD, Caemmerers S, Berry JA ( 1980). A biochemical model of photosynthetic CO₂ assimilation in leaves of C₃ species. Planta, 149, 78-90. DOI URL PMID
13	Fila G, Badeck FW, Meyer S, Cerovic Z, Ghashghaie J ( 2006). Relationships between leaf conductance to CO₂ diffusion and photosynthesis in micropropagated grapevine plants, before and after ex vitro acclimatization. Journal of Experimental Botany, 57, 2687-2695. DOI URL PMID
14	Gao S, Yan Q, Chen L, Song Y, Li J, Fu C, Dong M ( 2017 a). Effects of ploidy level and haplotype on variation of photosynthetic traits: Novel evidence from two Fragaria species. PLOS ONE, 12, e0179899. DOI: 10.1371/journal.? pone.0179899. DOI URL PMID
15	Gao Y, Xia JB, Chen YP, Zhao YY, Kong QX, Lang Y ( 2017b). Effects of extreme soil water stress on photosynthetic efficiency and water consumption characteristics of Tamarix chinensis in China’s Yellow River Delta. Journal of Forestry Research, 28, 491-501. DOI URL
16	Guo W, Zhan SY, Yin H, Li XY, Lü X, Yang L, Wang Y ( 2016). Effect of enhanced UV-B radiation on photosynthetic electron transport and light response characteristics of japonica. Journal of Nanjing Agricultural University, 39, 603-610. DOI URL
	[ 郭巍, 战莘晔, 殷红, 李雪莹, 吕晓, 杨璐, 王一 ( 2016). UV-B辐射增强对粳稻光合电子传递与光响应特性的影响. 南京农业大学学报, 39, 603-610.] DOI URL
17	Harley PC, Sharkey TD ( 1991). An improved model of C₃ photosynthesis at high CO₂: Reversed O₂ sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynthesis Research, 27, 169-178. DOI URL PMID
18	Hu WH, Ye ZP, Yan XH, Yang XS ( 2017). PSII function and intrinsic characteristics of light-harvesting pigment molecules for sun- and shading-leaf in Magnolia grandiflora during overwintering. Bulletin of Botanical Research, 37, 281-287.
	[ 胡文海, 叶子飘, 闫小红, 杨旭升 ( 2017). 越冬期广玉兰阳生叶和阴生叶PSII功能及捕光色素分子内禀特性的比较研究. 植物研究, 37, 281-287.]
19	Je?ilová E, No?ková-Hlavá?ková V, Duchoslav M ( 2015). Photosynthetic characteristics of three ploidy levels of Allium oleraceum L. (Amaryllidaceae) differing in ecological amplitude. Plant Species Biology, 30, 212-224. DOI URL
20	Kang HJ, Li H, Tao YL, Zhang HL, Quan W, Ouyang Z ( 2015). Discussion on simultaneous measurements of leaf gas exchange and chlorophyll fluorescence for estimating photosynthetic electron allocation. Acta Ecologica Sinica, 35, 1217-1224. DOI URL
	[ 康华靖, 李红, 陶月良, 张海利, 权伟, 欧阳竹 ( 2015). 气体交换与荧光同步测量估算植物光合电子流的分配. 生态学报, 35, 1217-1224.] DOI URL
21	Kirchhoff H, Haase W, Wegner S, Danielsson R, Ackermann R, Albertsson P ( 2007). Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplasts. Biochemistry, 46, 11169-11176. DOI URL
22	Leng HB, Qin J, Ye K, Feng SC, Gao K ( 2014). Comparison of light response models of photosynthesis in Nelumbo nucifera leaves under different light conditions. Chinese Journal of Applied Ecology, 25, 2855-2860.
	[ 冷寒冰, 秦俊, 叶康, 奉树成, 高凯 ( 2014). 不同光照环境下荷花叶片光合光响应模型比较. 应用生态学报, 25, 2855-2860.]
23	Li XN, Brestic M, Tan DX, Zivcak M, Zhu XC, Liu SQ, Song FB, Reiter RJ, Liu FL ( 2018). Melatonin alleviates low PSI-limited carbon assimilation under elevated CO₂ and enhances the cold tolerance of offspring in chlorophyll b-deficient mutant wheat. Journal of Pineal Research, 64, DOI: 10.1111/jpi.12453. DOI URL PMID
24	Li XN, Hao CL, Zhong JW, Liu FL, Cai J, Wang X, Zhou Q, Dai TB, Cao WX, Jiang D ( 2015). Mechano-stimulated modifications in the chloroplast antioxidant system and proteome changes are associated with cold response in wheat. BMC Plant Biology, 15, 1-13. DOI URL PMID
25	Liang XY, Liu SR ( 2017). A review on the FvCB biochemical model of photosynthesis and the measurement of A-C_i curves. Chinese Journal of Plant Ecology, 41, 693-706. DOI URL
	[ 梁星云, 刘世荣 ( 2017). FvCB生物化学光合模型及A-C_i曲线测定. 植物生态学报, 41, 693-706.] DOI URL
26	Long SP, Bernacchi CJ ( 2003). Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany, 54, 2393-2401. DOI URL PMID
27	Mayoral C, Calama R, Sánchez-González M, Pardos M ( 2015). Modelling the influence of light, water and temperature on photosynthesis in young trees of mixed Mediterranean forests. New Forests, 46, 485-506. DOI URL
28	Miao Z, Xu M, Lathrop RG, Wang Y ( 2009). Comparison of the A-C_c curve fitting methods in determining maximum ribulose-1,5-bisphosphate carboxylase/oxygenase carboxylation rate, potential light saturated electron transport rate and leaf dark respiration. Plant, Cell & Environment, 32, 109-122.
29	Niyogi KK, Truong TB ( 2013). Evolution of flexible non-?photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Current Opinion in Plant Biology, 16, 307-314. DOI URL PMID
30	Park KS, Bekhzod K, Kwon JK, Son JE ( 2016). Development of a coupled photosynthetic model of sweet basil hydroponically grown in plant factories. Horticulture, Environment and Biotechnology, 57, 20-26. DOI URL
31	Quiroz R, Loayza H, Barreda C, Gavilán C, Posadas A, Ramírez DA ( 2017). Linking process-based potato models with light reflectance data: Does model complexity enhance yield prediction accuracy? European Journal of Agronomy, 82, 104-112. DOI URL
32	Ralph PJ, Gademann R ( 2005). Rapid light curves: A powerful tool to assess photosynthetic activity. Aquatic Botany, 82, 222-237. DOI URL
33	Ser?dio J, Ezequiel J, Frommlet J, Laviale M, Lavaud J ( 2013). A method for the rapid generation of nonsequential light-response curves of chlorophyll fluorescence. Plant Physiology, 163, 1089-1102. DOI URL PMID
34	Shimada A, Kubo T, Tominaga S, Yamamoto M ( 2017). Effect of temperature on photosynthesis characteristics in the passion fruits ‘Summer Queen’ and ‘Ruby Star’. The Horticulture Journal, 86, 194-199. DOI URL
35	Smith E ( 1937). The influence of light and carbon dioxide on photosynthesis. Journal of General Physiology, 20, 807-830. DOI URL PMID
36	Sun J, Sun J, Feng Z ( 2015). Modelling photosynthesis in flag leaves of winter wheat (Triticum aestivum) considering the variation in photosynthesis parameters during developpment. Functional Plant Biology, 42, 1036-1044. DOI URL
37	Takahashi S, Badger M ( 2011). Photoprotection in plants: A new light on photosystem II damage. Trends in Plant Sciences, 16, 53-59. DOI URL PMID
38	Tang XL, Cao YH, Gu LH, Zhou BZ ( 2017a). Advances in photo-physiological responses of leaves to environmental factors based on the FvCB model. Acta Ecologica Sinica, 37, 6633-6645.
	[ 唐星林, 曹永慧, 顾连宏, 周本智 ( 2017a). 基于FvCB模型的叶片光合生理对环境因子的响应研究进展. 生态学报, 37, 6633-6645.]
39	Tang XL, Zhou BZ, Zhou Y, Ni X, Cao YH, Gu LH ( 2017b). Photo-physiological and photo-biochemical characteristics of several herbaceous and woody species based on FvCB model. Chinese Journal of Applied Ecology, 28, 1482-1488.
	[ 唐星林, 周本智, 周燕, 倪霞, 曹永慧, 顾连宏 ( 2017b). 基于FvCB模型的几种草本和木本植物光合生理生化特性. 应用生态学报, 28, 1482-1488.]
40	Thornley JHM ( 1976). Mathematical Models in Plant Physiology. Academic Press, London. 86-110.
41	Valentini R, Epron D, de Angelis P, Matteucci G, Dreyer E ( 1995). In situ estimation of net CO₂ assimilation, photosynthetic electron flow and photorespiration in Tukey oak (Q. cerris L.) leaves: Diurnal cycles under different levels of water supply. Plant, Cell & Environment, 18, 631-640. DOI URL
42	von Caemmerer S ( 2000). Biochemical Models of Leaf Photosynthesis. Techniques in Plant Sciences No. 2. Collingwood. CSIRO Publishing, Australia, Victoria.
43	von Caemmerer S ( 2013). Steady-state models of photosynthesis. Plant, Cell & Environment, 36, 1617-1630. DOI URL PMID
44	von Caemmerer S, Farquhar GD ( 1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 153, 376-387. DOI URL
45	Wang HZ, Han L, Xu YL, Niu JL, Yu J ( 2017). Simulated photosynthetic responses of Populus euphratica during drought stress using light-response models. Acta Ecologica Sinica, 37, 2315-2324. DOI URL
	[ 王海珍, 韩路, 徐雅丽, 牛建龙, 于军 ( 2017). 干旱胁迫下胡杨光合光响应过程模拟与模型比较. 生态学报, 37, 2315-2324.] DOI URL
46	Wang RR, Xia JB, Yang JH, Zhao YY, Liu JT, Sun JK ( 2013). Comparison of light response models of photosynthesis in leaves of Periploca sepium under drought stress in sand habitat formed from seashells. Chinese Journal of Plant Ecology, 37, 111-121. DOI URL
	[ 王荣荣, 夏江宝, 杨吉华, 赵艳云, 刘京涛, 孙景宽 ( 2013). 贝壳砂生境干旱胁迫下杠柳叶片光合光响应模型比较. 植物生态学报, 37, 111-121.] DOI URL
47	White AJ, Critchley C ( 1999). Rapid light curves: A new fluorescence method to asses the state of the photosynthetic apparatus. Photosynthesis Research, 59, 63-72. DOI URL
48	Ye ZP ( 2007). A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa. Photosynthetica, 45, 637-640. DOI URL
49	Ye ZP, Hu WH, Xiao YA, Fan DY, Yi JH, Duan SH, Yan XH, He L, Zhang SS ( 2014). A mechanistic model of light-response of photosynthetic electron flow and its application. Chinese Journal of Plant Ecology, 38, 1241-1249. DOI URL
	[ 叶子飘, 胡文海, 肖宜安, 樊大勇, 尹建华, 段世华, 闫小红, 贺俐, 张斯斯 ( 2014). 光合电子流对光响应的机理模型及其应用. 植物生态学报, 38, 1241-1249.] DOI URL
50	Ye ZP, Robakowski P, Suggett JD ( 2013a). A mechanistic model for the light response of photosynthetic electron transport rate based on light harvesting properties of photosynthetic pigment molecules. Planta, 237, 837-847. DOI URL PMID
51	Ye ZP, Suggett JD, Robakowski P, Kang HJ ( 2013b). A mechanistic model for the photosynthesis-light response based on the photosynthetic electron transport of PSII in C₃ and C₄ species. New Phytologist, 152, 1251-1262. DOI URL PMID
52	Yin XY, Struik PC, Romero P, Harbinson J, Evers JB, van der Putten PEL, Vos J ( 2009). Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C₃ photosynthesis model: A critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy. Plant, Cell & Environment, 32, 448-464.

参数 Parameter	处理 Treatment
	遮阴 Shading			全日照 Full sunlight
	模型I Model I	模型II Model II	测量值 Observed value	模型I Model I	模型II Model II	测量值 Observed value
最大电子传递速率 Maximum electron transport rate (J_max, mmol·m^-2·s^-1)	269.13 ± 5.22^a	236.68 ± 1.39^b	?236.29	354.26 ± 17.73^a	307.91 ± 8.95^b	?306.43
饱和光强 Saturated light intensity (PAR_sat, mmol·m^-2·s^-1)	—	1 839.98 ± 50.53	?1 800	—	1 967.69 ± 110.64	?2 000
确定系数 Determination coefficient (R²)	0.999	0.999	—	0.999	0.999	—

参数 Parameter	处理 Treatment
	遮阴 Shading			全日照 Full sunlight
	模型I Model I	模型II Model II	测量值 Observed value	模型I Model I	模型II Model II	测量值 Observed value
最大电子传递速率 Maximum electron transport rate (J_max, mmol·m^-2·s^-1)	269.13 ± 5.22^a	236.68 ± 1.39^b	?236.29	354.26 ± 17.73^a	307.91 ± 8.95^b	?306.43
饱和光强 Saturated light intensity (PAR_sat, mmol·m^-2·s^-1)	—	1 839.98 ± 50.53	?1 800	—	1 967.69 ± 110.64	?2 000
确定系数 Determination coefficient (R²)	0.999	0.999	—	0.999	0.999	—

参数 Parameter	处理 Treatment
	遮阴 Shading			全日照 Full sunlight
	模型I Model I	模型II Model II	测量值 Observed value	模型I Model I	模型II Model II	测量值 Observed value
初始斜率 Initial slope of A-I curve, α (mmol·mol^-1)	0.061 ± 0.044^b	0.081 ± 0.032^a	-	0.064 ± 0.025^a	0.069 ± 0.025^a	-
最大净光合速率 Maximum net photosynthetic rate, A_nmax(mmol·m^-2·s^-1)	31.28 ± 1.33^a	26.92 ± 1.23^b	?27.23	45.56 ± 1.41^a	35.52 ± 1.26^b	?36.17
饱和光强 Saturated irradiance, I_sat(mmol ·m^-2·s^-1)	-	1 569.96 ± 24.89	?1 600	-	1 998.36 ± 36.45	?1 800
光补偿点 Light compensation point, I_c(mmol·m^-2·s^-1)	40.65 ± 2.85^a	40.83 ± 2.74^a	?41.59	51.49 ± 3.52^a	51.62 ± 3.45^a	?51.96
暗呼吸速率 Dark respiration, R_d(mmol·m^-2 ·s^-1)	2.42 ± 0.87^b	2.99 ± 0.58^a	?3.12	3.19 ± 0.56^a	3.45 ± 0.42^a	?3.51
确定系数 Determination coefficient, R²	0.999	0.999	0.999	0.999	0.999	0.999

参数 Parameter	处理 Treatment
	遮阴 Shading			全日照 Full sunlight
	模型I Model I	模型II Model II	测量值 Observed value	模型I Model I	模型II Model II	测量值 Observed value
初始斜率 Initial slope of A-I curve, α (mmol·mol^-1)	0.061 ± 0.044^b	0.081 ± 0.032^a	-	0.064 ± 0.025^a	0.069 ± 0.025^a	-
最大净光合速率 Maximum net photosynthetic rate, A_nmax(mmol·m^-2·s^-1)	31.28 ± 1.33^a	26.92 ± 1.23^b	?27.23	45.56 ± 1.41^a	35.52 ± 1.26^b	?36.17
饱和光强 Saturated irradiance, I_sat(mmol ·m^-2·s^-1)	-	1 569.96 ± 24.89	?1 600	-	1 998.36 ± 36.45	?1 800
光补偿点 Light compensation point, I_c(mmol·m^-2·s^-1)	40.65 ± 2.85^a	40.83 ± 2.74^a	?41.59	51.49 ± 3.52^a	51.62 ± 3.45^a	?51.96
暗呼吸速率 Dark respiration, R_d(mmol·m^-2 ·s^-1)	2.42 ± 0.87^b	2.99 ± 0.58^a	?3.12	3.19 ± 0.56^a	3.45 ± 0.42^a	?3.51
确定系数 Determination coefficient, R²	0.999	0.999	0.999	0.999	0.999	0.999

参数 Parameter	处理 Treatment
	遮阴 Shading			全日照 Full sunlight
	模型I Model I	模型II Model II	测量或计算值 Observed value	模型I Model I	模型II Model II	测量或计算值 Observed value
最大电子传递速率 Maximum electron transport rate, J_max(mmol·m^-2·s^-1)	269.13^a	236.68^b	236.29^b	354.26^a	307.91^b	306.43^b
最大净光合速率 Maximum net photosynthetic rate, A_nmax(mmol·m^-2·s^-1)	31.28^a	26.92^b	27.23^b	45.56^a	35.52^b	36.17^b
碳同化电子流 Electron flow of partitioning C assimilation, J_C-max (mmol·m^-2·s^-1)	166.48^a	155.67^a	155.54^a	219.23^a	203.78^a	203.26^a
光呼吸电子流 Electron flow of partitioning photorespiration assimilation, J_O-max (mmol·m^-2·s^-1)	102.65^a	81.01^b	80.75^b	135.03^a	104.13^b	103.17^b