Effects of potassium deficiency on photosynthesis, chloroplast ultrastructure, ROS, and antioxidant activities in maize (Zea mays L.)

doi:10.1016/S2095-3119(18)61953-7

摘要/Abstract

Abstract:

Potassium (K) deficiency significantly decreases photosynthesis due to leaf chlorosis induced by accumulation of reactive oxygen species (ROS). But, the physiological mechanism for adjusting antioxidative defense system to protect leaf function in maize (Zea mays L.) is unknown. In the present study, four maize inbred lines (K-tolerant, 90-21-3 and 099; K-sensitive, D937 and 835) were used to analyze leaf photosynthesis, anatomical structure, chloroplast ultrastructure, ROS, and antioxidant activities. The results showed that the chlorophyll content, net photosynthetic rate (P_n), stomatal conductance (G_s), photochemical quenching (q_P), and electron transport rate of PSII (ETR) in 90-21-3 and 099 were higher than those in D937 and 835 under K deficiency treatment. Parameters of leaf anatomical structure in D937 that were significantly changed under K deficiency treatment include smaller thickness of leaf, lower epidermis cells, and vascular bundle area, whereas the vascular bundle area, xylem vessel number, and area in 90-21-3 were significantly larger or higher. D937 also had seriously damaged chloroplasts and PSII reaction centers along with increased superoxide anion (O₂^-·) and hydrogen peroxide (H₂O₂). Activities of antioxidants, like superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX), were significantly stimulated in 90-21-3 resulting in lower levels of O₂^-· and H₂O₂. These results indicated that the K-tolerant maize promoted antioxidant enzyme activities to maintain ROS homeostasis and suffered less oxidative damage on the photosynthetic apparatus, thereby maintaining regular photosynthesis under K deficiency stress.

Key words: potassium deficiency , maize,, photosynthesis , chloroplast ultrastructure , ROS and antioxidant

. [J]. Journal of Integrative Agriculture, 2019, 18(2): 395-406.

DU Qi, ZHAO Xin-hua, XIA Le, JIANG Chun-ji, WANG Xiao-guang, HAN Yi, WANG Jing, YU Hai-qiu. Effects of potassium deficiency on photosynthesis, chloroplast ultrastructure, ROS, and antioxidant activities in maize (Zea mays L.)[J]. Journal of Integrative Agriculture, 2019, 18(2): 395-406.

参考文献

Ahanger M A, Agarwal R M. 2017. Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma, 254, 1471–1486.
Akcay U C, Ercan O, Kavas M, Yildiz L, Yilmaz C, Oktem H A, Yucel M. 2010. Drought-induced oxidative damage and antioxidant responses in peanut (Arachis hypogaea L.) seedlings. Plant Growth Regulation, 61, 21–28.
Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 728–749.
Bednarz C W, Oosterhuis D M, Evans R D. 1998. Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environmental & Experimental Botany, 39, 131–139.
Bilger W, Björkman O. 1990. Role of xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research, 25, 173–185.
Cakmak I. 2005. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science, 168, 521–530.
Cao M J, Yu H Q, Yan H K, Jiang C J. 2007. Difference in tolerance to potassium deficiency between two maize inbred lines. Plant Production Science, 10, 42–46.
Chawla S, Jain S, Jain V. 2013. Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). Journal of Plant Biochemistry & Biotechnology, 22, 27–34.
Chen P, Mitsui T, Farmer D B, GolovchenkoJ, Gordon R G, Branton D. 2004. Atomic layer deposition to fine-tune the surface properties and diameters of fabricated nanopores. Nano Letters, 4, 1333–1337.
Chen S, Zhao H, Ding G, Xu F. 2015. Genotypic differences in antioxidant response to phosphorus deficiency in Brassica napus. Plant and Soil, 391, 19–32.
Chen W, Yang X, He Z, Feng Y, Hu F. 2008. Differential changes in photosynthetic capacity, 77 K chlorophyll fluorescence and chloroplast ultrastructure between Zn-efficient and Zn-inefficient rice genotypes (Oryza sativa) under low zinc stress. Physiologia Plantarum, 132, 89–101.
Foyer C H, Noctor G. 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell, 17, 1866–1875.
Garratt L, Janagoudar B, Lowe K, Anthony P, Power J, Davey M. 2002. Salinity tolerance and antioxidant status in cotton cultures. Free Radical Biology & Medicine, 33, 502–511.
Hernandez M, Fernandez-Garcia N, Garcia-Garma J, Rubio-Asensio J S, Rubio F, Olmos E. 2012. Potassium starvation induces oxidative stress in Solanum lycopersicum L. roots. Journal of Plant Physiology, 169, 1366–1374.
Hu W, Coomer T D, Loka D A, Oosterhuis D M, Zhou Z. 2017. Potassium deficiency affects the carbon-nitrogen balance in cotton leaves. Plant Physiology & Biochemistry, 115, 408.
Hu W, Lv X, Yang J, Chen B, Zhao W, Meng Y, Wang Y, Zhou Z, Oosterhuis D M. 2016. Effects of potassium deficiency on antioxidant metabolism related to leaf senescence in cotton (Gossypium hirsutum L.). Field Crops Research, 191, 139–149.
Jia Y, Yang X, Islam E, Feng Y. 2007. Effects of potassium deficiency on chloroplast ultrastructure and chlorophyll fluorescence in inefficient and efficient genotypes of rice. Journal of Plant Nutrition, 31, 2105–2118.
Kalaji H M, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska I A, Cetner M D, Allakhverdiev S I, Goltsev V. 2014. Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiology & Biochemistry, 81, 16–25.
Kim M J, Ciani S, Schachtman D P. 2010. A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Molecular Plant, 3, 420–427.
Lawanson A O, Otusanya O O, Akomolede D A. 1977. Mechanism of potassium deficiency-induced retardation of chlorophyll biosynthesis in Zea mays. Experientia, 33, 1145–1146.
Li C L, Wang Y Q, Liu L C, Hu Y C, Zhang F X, Mergen S, Wang G D, Schläppi M R, Chu C C. 2011. A rice plastidial nucleotide sugar epimerase is involved in galactolipid biosynthesis and improves photosynthetic efficiency. PLoS Genetics, 7, e1002196.
Li M, Zhao Z, Zhang Z, Zhang W, Zhou J, Xu F, Liu X. 2017. Effect of boron deficiency on anatomical structure and chemical composition of petioles and photosynthesis of leaves in cotton (Gossypium hirsutum L.). Scientific Reports, 7, 4420.
Li X T, Cao P, Wang X G, Cao M J, Yu H Q. 2011. Comparison of gas exchange and chlorophyll fluorescence of low-potassium-tolerant and -sensitive soybean [Glycine max (L.) Merr.] cultivars under low-potassium condition. Photosynthetica, 49, 633–636.
Lu Z, Ren T, Pan Y, Li X, Cong R, Lu J. 2016. Differences on photosynthetic limitations between leaf margins and leaf centers under potassium deficiency for Brassica napus L. Scientific Reports, 6, 21725.
Mattiello E M, Ruiz H A, Neves J C, Ventrella M C, Araújo W L. 2015. Zinc deficiency affects physiological and anatomical characteristics in maize leaves. Journal of Plant Physiology, 183, 138–143.
Mir B A, Mir S A, Khazir J, Tonfack L B, Cowan D A, Vyas D, Koul S. 2015. Cold stress affects antioxidative response and accumulation of medicinally important withanolides in Withania somnifera (L.) Dunal. Industrial Crops & Products, 74, 1008–1016.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science, 9, 490–498.
Neto A D D A, Prisco J T, Enéas-Filho J, Abreu C E B D, Gomes-Filho E. 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environmental & Experimental Botany, 56, 87–94.
Qi J, Wang J, Gong Z, Zhou J M. 2017. Apoplastic ROS signaling in plant immunity. Current Opinion in Plant Biology, 38, 92–100.
Qu C, Liu C, Ze Y, Gong X, Hong M, Wang L, Hong F. 2011. Inhibition of nitrogen and photosynthetic carbon assimilation of maize seedlings by exposure to a combination of salt stress and potassium-deficient stress. Biological Trace Element Research, 144, 1159–1174.
Ren B, Zhang J, Dong S, Liu P, Zhao B. 2016. Effects of waterlogging on leaf mesophyll cell ultrastructure and photosynthetic characteristics of summer maize. PLoS ONE, 11, e0161424.
del Río L A. 2015. ROS and RNS in plant physiology: An overview. Journal of Experimental Botany, 66, 2827–2837.
Römheld V, Kirkby E A. 2010. Research on potassium in agriculture: Needs and prospects. Plant and Soil, 335, 155–180.
Ruan L, Zhang J, Xin X, Zhang C, Ma D, Chen L, Zhao B. 2015. Comparative analysis of potassium deficiency-responsive transcriptomes in low potassium susceptible and tolerant wheat (Triticum aestivum L.). Scientific Reports, 5, 10090.
Shao Q, Wang H, Guo H, Zhou A, Huang Y, Sun Y, Li M. 2014. Effects of shade treatments on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii. PLoS ONE, 9, e85996.
Shao R X, Xin L F, Zheng H F, Li L L, Ran W L, Mao J, Yang Q H. 2016. Changes in chloroplast ultrastructure in leaves of drought-stressed maize inbred lines. Photosynthetica, 54, 74–80.
Shin R, Berg R H, Schachtman D P. 2005. Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant & Cell Physiology, 46, 1350–1357.
Shin R, Schachtman D P. 2004. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proceedings of the National Academy of Sciences of the United States of America, 101, 8827–8832.
Sun Z, Chen Y, Schaefer V, Liang H, Li W, Huang S, Peng C. 2015. Responses of the hybrid between sphagneticola trilobata and sphagneticola calendulacea to low temperature and weak light characteristic in south China. Scientific Reports, 5, 16906
Tian M, Gu Q, Zhu M. 2003. The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus. Plant Science, 165, 701–707.
Tian X L, Wang G W, Zhu R, Yang P Z, Duan L S, Li Z H. 2008. Conditions and Indicators for screening cotton (Gossypium hirsutum L.) varieties tolerant to low potassium. Acta Agronomica Sinica, 34, 1435–1443. (in Chinese)
Tsai Y C, Hong C Y, Liu L F, Kao C H. 2004. Relative importance of Na+ and Cl– in NaCl-induced antioxidant systems in roots of rice seedlings. Physiologia Plantarum, 90, 86–94.
Veronica N, Subrahmanyam D, Vishnu Kiran T, Yugandhar P, Bhadana V P, Padma V, Jayasree G, Voleti S R. 2017. Influence of low phosphorus concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynthetica, 55, 285–293.
Wang X G, Zhao X H, Jiang C J, Li C H, Cong S, Wu D, Chen Y Q, Yu H Q, Wang C Y. 2015. Effects of potassium deficiency on photosynthesis and photoprotection mechanisms in soybean (Glycine max (L.) Merr.). Journal of Integrative Agriculture, 14, 856–863.
Wang X L, Yu H Q, Liu N, Yi B, Cao M J. 2012. Physiological characteristics of delaying leaf senescence in maize inbred lines tolerant to potassium deficiency. Acta Agronomica Sinica, 38, 1672–1679. (in Chinese)
Wang Y, Wu W H. 2017. Regulation of potassium transport and signaling in plants. Current Opinion in Plant Biology, 39, 123–128.
Xu P L, Guo Y K, Bai J G, Shang L, Wang X J. 2008. Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiologia Plantarum, 132, 467–478.
Xu S, Li J, Zhang X, Wei H, Cui L. 2006. Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environmental & Experimental Botany, 56, 274–285.
You J, Chan Z. 2015. ROS regulation during abiotic stress responses in crop plants. Frontiers in Plant Science, 6, 1092.
Zhao D, Oosterhuis D M, Bednarz C W. 2001. Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosynthetica, 38, 103–109.
Zhao X H, Yu H Q, Wen J, Wang X G, Du Q, Wang J, Wang Q. 2016. Response of root morphology, physiology and endogenous hormones in maize (Zea mays L.) to potassium deficiency. Journal of Integrative Agriculture, 15, 785–794.