Heterologous expression of HpBHY and CrBKT increases heat tolerance in Physcomitrella patens

doi:10.1016/j.pld.2019.04.001

Abstract

Abstract: Heat stress can restrict plant growth, development, and crop yield. As essential plant antioxidants, carotenoids play significant roles in plant stress resistance. b-carotene hydroxylase (BHY) and b-carotene ketolase (BKT), which catalyze the conversions of b-carotene to zeaxanthin and b-carotene to canthaxanthin, respectively, are key enzymes in the carotenoid biosynthetic pathway, but little is known about their potential functions in stress resistance. Here, we investigated the roles of b-carotene hydroxylase and b-carotene ketolase during heat stress in Physcomitrella patens through expressing a b-carotene ketolase gene from Chlamydomonas reinhardtii (CrBKT) and a b-carotene hydroxylase gene from Haematococcus pluvialis (HpBHY) in the moss P. patens. In transgenic moss expressing these genes, carotenoids content increased (especially lutein content), and heat stress tolerance increased, with reduced leafy tissue necrosis. To investigate the mechanism of this heat stress resistance, we measured various physiological indicators and found a lower malondialdehyde level, higher peroxidase and superoxide dismutase activities, and higher endogenous abscisic acid and salicylate content in the transgenic plants in response to high-temperature stress. These results demonstrate that CrBKT and HpBHY increase plant heat stress resistance through the antioxidant and damage repair metabolism, which is related to abscisic acid and salicylate signaling.

Key words: Carotenoids, Heat stress, Antioxidant, Abscisic acid, Physcomitrella patens

Jianfang He, Ping Li, Heqiang Huo, Lina Liu, Ting Tang, Mingxia He, Junchao Huang, Li Liu. Heterologous expression of HpBHY and CrBKT increases heat tolerance in Physcomitrella patens[J]. Plant Diversity, 2019, 41(04): 266-274.

Figures/Tables 5

References 44

[1]	Abera G, Wolde-meskel E, Bakken LR (2012). Carbon and nitrogen mineralization dynamics in different soils of the tropics amended with legume residues and contrasting soil moisture contents.Biology and Fertility of Soils, 48, 51-66.
[2]	Blagodatskaya E, Kuzyakov Y (2008). Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: Critical review.Biology and Fertility of Soils, 45, 115-131.
[3]	Bu XL, Ding JM, Wang LM, Yu XN, Huang W, Ruan HH (2011). Biodegradation and chemical characteristics of hot-water extractable organic matter from soils under four different vegetation types in the Wuyi Mountains, southeastern China.European Journal of Soil Biology, 47, 102-107.
[4]	Chen GS, Yang ZJ, Gao R, Xie JS, Guo JF, Huang ZQ, Yang YS (2013). Carbon storage in a chronosequence of Chinese fir plantations in southern China.Forest Ecology and Management, 300, 68-76.
[5]	Cheng WX, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2014). Synthesis and modeling perspectives of rhizosphere priming.New Phytologist, 201, 31-44.
[6]	Cleveland CC, Neff JC, Townsend AR, Hood E (2004). Composition, dynamics, and fate of leached dissolved organic matter in terrestrial ecosystems: Results from a decomposition experiment.Ecosystems, 7, 175-285.
[7]	Cleveland CC, Wieder WR, Reed SC, Townsend AR (2010). Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere.Ecology, 91, 2313-2323.
[8]	Eswaran H, van Den Berg E, Reich P (1993). Organic carbon in soils of the world.Soil Science Society of America Journal, 57, 192-194.
[9]	Fierer N, Craine JM, McLauchlan K, Schimel JP (2005). Litter quality and the temperature sensitivity of decomposition.Ecology, 86, 320-326.
[10]	Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004). Carbon input to soil may decrease soil carbon content.Ecology Letters, 7, 314-320.
[11]	Fujii K, Hayakawa C, van Hees PA, Funakawa S, Kosaki T (2010). Biodegradation of low molecular weight organic compounds and their contribution to heterotrophic soil respiration in three Japanese forest soils.Plant and Soil, 334, 475-489.
[12]	Gauthier A, Amiotte-Suchet P, Nelson PN, Lévêque J, Zeller B, Hénault C (2010). Dynamics of the water extractable organic carbon pool during mineralisation in soils from a Douglas fir plantation and an oak-beech forest―An incubation experiment.Plant and Soil, 330, 465-479.
[13]	Haken H, Wolf HC (1995). Molecular Physics and Elements of Quantum Chemistry. Springer-Verlag, Berlin.
[14]	Hartley IP, Ineson P (2008). Substrate quality and the temperature sensitivity of soil organic matter decomposition.Soil Biology & Biochemistry, 40, 1567-1574.
[15]	He DM, Ruan HH (2014). Long term effect of land reclamation from Lake on chemical composition of soil organic matter and its mineralization.PLoS ONE, 9, e99251.
[16]	Hoosbeek MR, Scarascia-Mugnozza GE (2009). Increased litter build up and soil organic matter stabilization in a poplar plantation after 6 years of atmospheric CO2 enrichment (FACE): Final results of POP-Euro FACE compared to other forest FACE experiments.Ecosystems, 12, 220-239.
[17]	Inamdar S, Finger N, Singh S, Mitchell M, Levia D, Bais H, Scott D, McHale P (2012). Dissolved organic matter (DOM) concentration and quality in a forested mid- Atlantic watershed, USA.Biogeochemistry, 108, 55-76.
[18]	Kalbitz K, Meyer A, Yang R, Gerstberger P (2007). Response of dissolved organic matter in the forest floor to long-term manipulation of litter and throughfall inputs.Biogeochemistry, 86, 301-318.
[19]	Kang GL, Yang YS, Si YT, Yin YF, Liu Z, Chen GS, Yang ZJ (2014). Quantities and spectral characteristics of DOM released from leaf and litterfall in Castanopsis carlesii forest and Cunninghamia lanceolata plantation.Acta Ecologica Sinica, 34, 1946-1955.(in Chinese with English abstract) [康根丽, 杨玉盛, 司友涛, 尹云锋, 刘翥, 陈光水, 杨智杰 (2014). 米槠人促更新林与杉木人工林叶片及凋落物溶解性有机物的数量和光谱学特征. 生态学报, 34, 1946-1955.]
[20]	Kiikkilä O, Kitunen V, Smolander A (2011). Properties of dissolved organic matter derived from silver birch and Norway spruce stands: Degradability combined with chemical characteristics.Soil Biology & Biochemistry, 43, 421-430.
[21]	Kiikkilä O, Kitunen V, Spetz P, Smolander A (2012). Characterization of dissolved organic matter in decomposing Norway spruce and silver birch litter.European Journal of Soil Science, 63, 476-486.
[22]	Kiikkilä O, Kanerva S, Kitunen V, Smolander A (2014). Soil microbial activity in relation to dissolved organic matter properties under different tree species.Plant and Soil, 377, 169-177.
[23]	Kirschbaum MUF (2004). Soil respiration under prolonged soil warming: Are rate reductions caused by acclimation or substrate loss?Global Change Biology, 10, 1870-1877.
[24]	Kothawala DN, Roehm C, Blodau C, Moore TR (2012). Selective adsorption of dissolved organic matter to mineral soils. Geoderma, 189-190, 334-342.
[25]	Kuzyakov Y (2010). Priming effects: Interactions between living and dead organic matter.Soil Biology & Biochemistry, 42, 1363-1371.
[26]	Kuzyakov Y, Friedel JK, Stahr K (2000). Review of mechanisms and quantification of priming effects.Soil Biology & Biochemistry, 32, 1485-1498.
[27]	Leff JW, Nemergut DR, Grandy AS, O’Neill SP, Wickings K, Townsend AR, Cleveland CC (2012). The effects of soil bacterial community structure on decomposition in a tropical rain forest.Ecosystems, 15, 284-298.
[28]	Li ZP, Han CW, Han FX (2010). Organic C and N mineralization as affected by dissolved organic matter in paddy soils of subtropical China.Geoderma, 157, 206-213.
[29]	Marschner B, Kalbitz K (2003). Controls of bioavailability and biodegradability of dissolved organic matter in soils.Geoderma, 113, 211-235.
[30]	Nourbakhsh F, Dick RP (2005). Net nitrogen mineralization or immobilization potential in a residue―Amended calcareous soil.Arid Land Research and Management, 19, 299-306.
[31]	Peuravuori J, Pihlaja K (1997). Molecular size distribution and spectroscopic properties of aquatic humic substances.Analytica Chimica Acta, 337, 133-149.
[32]	Qiao N, Schaefer D, Blagodatskaya E, Zou XM, Xu XL, Kuzyakov Y (2014). Labile carbon retention compensates for CO2 released by priming in forest soils.Global Change Biology, 20, 1943-1954.
[33]	Rousk J, Brookes PC, Glanville HC, Jones DL (2011). Lack of correlation between turnover of low-molecular-weight dissolved organic carbon and differences in microbial community composition or growth across a soil pH gradient.Applied and Environmental Microbiology, 77, 2791-2795.
[34]	Sun G, Luo P, Wu N, Qiu PF, Gao YH, Chen H, Shi FS (2009). Stellera chamaejasme L. increases soil N availability, turnover rates and microbial biomass in an alpine meadow ecosystem on the eastern Tibetan Plateau of China.Soil Biology & Biochemistry, 41, 86-91.
[35]	van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström US (2005). The carbon we do not see-the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: A review.Soil Biology & Biochemistry, 37, 1-13.
[36]	Vesterdal L, Elberling B, Christiansen JR, Callesen I, Schmidt IK (2012). Soil respiration and rates of soil carbon turnover differ among six common European tree species.Forest Ecology and Management, 264, 185-196.
[37]	Wang QK, Liu SP, Wang SL (2013). Debris manipulation alters soil CO2 efflux in a subtropical plantation forest.Geoderma, 192, 316-322.
[38]	Wang QK, Wang SL, He TX, Liu L, Wu JB (2014). Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils.Soil Biology & Biochemistry, 71, 13-20.
[39]	Wieder WR, Cleveland CC, Townsend AR (2008). Tropical tree species composition affects the oxidation of dissolved organic matter from litter.Biogeochemistry, 88, 127-138.
[40]	Wu JJ, Yang ZJ, Liu XF, Xiong DC, Lin WS, Chen CQ, Wang XH (2014). Analysis of soil respiration and components in Castanopsis carlesii and Cunninghamia lanceolata planta- tions.Chinese Journal of Plant Ecology, 38, 45-53.(in Chinese with English abstract) [吴君君, 杨智杰, 刘小飞, 熊德成, 林伟盛, 陈朝琪, 王小红 (2014). 米槠和杉木人工林土壤呼吸及其组分分析. 植物生态学报, 38, 45-53.]
[41]	Xiao Y, Zhou GY, Zhang QM, Wang WT, Liu SZ (2014). Increasing active biomass carbon may lead to a breakdown of mature forest equilibrium.Scientific Reports, 4, doi:10.1038/srep03681.
[42]	Xiong L, Yang YS, Wang QZ, Yang ZJ, Huang H, Si YT (2014). Movement of dissolved organic carbon in natural forest soil of Castanopsis carlesii.Journal of Subtropical Resources and Environment, 9(1), 46-52.(in Chinese with English abstract) [熊丽, 杨玉盛, 王巧珍, 杨智杰, 黄惠, 司友涛 (2014). 可溶性有机碳在米槠天然林土壤中的淋溶特征. 亚热带资源与环境学报, 9(1), 46-52.]
[43]	Yang K, Zhu JJ (2015). Impact of tree litter decomposition on soil biochemical properties obtained from a temperate secondary forest in Northeast China.Journal of Soils and Sediments, 15, 13-23.
[44]	Zhang HB (1993). Forest in Fujian. China Forestry Publishing House, Beijing.(in Chinese) [章浩白 (1993). 福建森林. 中国林业出版社, 北京.]

	可溶性有机碳 Dissolved organic carbon (g·kg^-1)	可溶性有机氮 Dissolved organic nitrogen (g·kg^-1)	紫外吸收值 Special ultraviolet visible absorption (UV)	腐殖化指标 Humification index (HIX)	分子量大小 Molecular size	pH
杉木鲜叶 Fresh leaves of Cunninghamia lanceolata	2.60 ± 0.51^a	0.005 ± 0.001^a	0.24 ± 0.01^a	0.26 ± 0.01^a	5.24 ± 0.98^a	5.98 ± 0.12^a
米槠鲜叶 Fresh leaves of Castanopsis carlesii	0.80 ± 0.11^b	0.024 ± 0.002^b	0.76 ± 0.08^b	1.75 ± 0.11^b	3.75 ± 0.10^b	5.91 ± 0.05^b
杉木凋落叶 Leaf litter of Cunninghamia lanceolata	0.99 ± 0.03^c	0.014 ± 0.001^c	1.61 ± 0.02^c	1.91 ± 0.03^c	6.90 ± 0.07^c	5.76 ± 0.05^c
米槠凋落叶 Leaf litter of Castanopsis carlesii	1.59 ± 0.02^d	0.020 ± 0.001^d	1.64 ± 0.04^c	1.90 ± 0.02^c	4.80 ± 0.30^d	4.28 ± 0.01^d

	可溶性有机碳 Dissolved organic carbon (g·kg^-1)	可溶性有机氮 Dissolved organic nitrogen (g·kg^-1)	紫外吸收值 Special ultraviolet visible absorption (UV)	腐殖化指标 Humification index (HIX)	分子量大小 Molecular size	pH
杉木鲜叶 Fresh leaves of Cunninghamia lanceolata	2.60 ± 0.51^a	0.005 ± 0.001^a	0.24 ± 0.01^a	0.26 ± 0.01^a	5.24 ± 0.98^a	5.98 ± 0.12^a
米槠鲜叶 Fresh leaves of Castanopsis carlesii	0.80 ± 0.11^b	0.024 ± 0.002^b	0.76 ± 0.08^b	1.75 ± 0.11^b	3.75 ± 0.10^b	5.91 ± 0.05^b
杉木凋落叶 Leaf litter of Cunninghamia lanceolata	0.99 ± 0.03^c	0.014 ± 0.001^c	1.61 ± 0.02^c	1.91 ± 0.03^c	6.90 ± 0.07^c	5.76 ± 0.05^c
米槠凋落叶 Leaf litter of Castanopsis carlesii	1.59 ± 0.02^d	0.020 ± 0.001^d	1.64 ± 0.04^c	1.90 ± 0.02^c	4.80 ± 0.30^d	4.28 ± 0.01^d