异源授粉山核桃果皮光合能力差异的转录组分析
|
摘要
【目的】探讨采用薄壳山核桃花粉授粉增强山核桃果皮光合能力的分子机理,为花粉直感的深入研究奠定基础。【方法】以山核桃花粉(记为hp)和薄壳山核桃花粉(记为pp)授粉的山核桃果皮为研究材料,在山核桃果实快速膨大期(授粉后65天,65DAP),对不同花粉授粉后山核桃果皮进行转录组测序,通过对叶绿素合成、光反应、碳同化等通路的基因富集分析,结合叶绿素含量、光合速率及光合关键酶活性的变化,筛选出增强山核桃果皮光合能力的相关基因。【结果】65DAP时,pp授粉的山核桃果皮中叶绿素含量、光合速率、1,5-二磷酸核酮糖羧化酶(Rubisco)活性、磷酸烯醇式丙酮酸羧化酶(PEPC)活性分别是hp授粉的1.31倍(P=0.047)、1.12倍(P=0.000 43)、1.65倍(P=0.036)和1.23倍(P=0.001 3)。转录组测序共产生32 908条scaffolds,并从1 894个差异基因(P<0.05,foldchange>1.5倍)中筛选出66个与山核桃果皮光合相关的基因,主要富集在叶绿素合成通路及光合固碳途径中,其中叶绿素合成途径中镁螯合酶编码基因(CHLH)、镁-原卟啉单甲酯环化酶编码基因(CRD)和叶绿素b还原酶编码基因(NYC)表达量明显上调,脱酶叶绿酸编码基因(PAO)表达量则显著下降;光合碳同化途径中有16个基因以及Rubisco活化酶编码基因(RCA)和碳酸酐酶编码基因(CA)表达量均明显上调;与光保护相关的42个基因表达量也明显上调。【结论】在山核桃果实快速膨大期,薄壳山核桃花粉授粉的山核桃果皮中的镁螯合酶编码基因(CHLH)、镁-原卟啉单甲酯环化酶编码基因(CRD)、叶绿素b还原酶编码基因(NYC)、捕光蛋白编码基因(LHCⅡ)、光修复相关蛋白编码基因(PSAN、PSAB27、STN7)和38个热激蛋白编码基因(HSP)、Rubisco活化酶编码基因(RCA)以及碳酸酐酶编码基因(CA)均显著上调,表明薄壳山核桃授粉的山核桃果皮光合能力的增强与其叶绿素合成、光能捕获和碳固定等光合作用相关通路的基因表达上调有关。
【Objective】To elucidate the molecular mechanism for enhancing photosynthetic capacity of the exocarp of Carya carthayensis fruits pollinated by Carya illinoensis in order to provide a theoretic basis for further research on metaxenia.【Method】 Transcriptome sequencing was performed for exocarp of C. cathayensis respectively pollinated by C. cathayensis(marked as hp) and C. illinoensis(marked as pp) with samples collected 65 days after pollination(65DAP) when the fruit rapidly expanding in size. Gene enrichment analysis was conducted for pathways of chlorophyll synthesis, photo-response and carbon assimilation in combination with variation in chlorophyll content, photosynthetic rate and activity of key enzymes involved in the photosynthesis.【Result】Compared to the fruit pollinated with hp, the chlorophyll content, photosynthetic rate, Rubisco activity, and phosphoenolpyruvate carboxylase(PEPC) activity of exocarp in the fruit pollinated with pp were 1.31(P=0.047), 1.12(P=0.000 43), 1.65(P=0.036), and 1.23(P=0.001 3) folds, respectively. A total of 32 908 scaffolds were generated by transcriptome sequencing, and 66 photosynthesis-related genes were screened from 1 894 differentially expressed genes(DEGs)(P <0.05,fold change>1.5), which were mainly involved in pathways of chlorophyll synthesis and photosynthetic carbon fixation. The expression of magnesium-chelatase subunit(CHLH), agnesium-protoporphyrin IX monomethyl ester [oxidative] cyclase(CRD), and chlorophyll(ide) b reductase(NYC) of the fruit pollinated with pp was significantly up-regulated while that of pheophorbide a oxygenase(PAO) was significantly down-regulated in the chlorophyll biosynthesis pathway, and the expression of 16 light harvesting pigment protein complexes(LHCⅡ)-coding genes, ribulose bisphosphate carboxylase/oxygenase activase(RCA), alpha carbonic anhydrase(CA) in the photosynthetic carbon fixation pathway were significantly up-regulated. 42 genes involved in photoprotection of exocarp are also showed significantly high expression in the fruit pollinated with pp than those in the fruit pollinated with hp.【Conclusion】 In the rapid growth period of Carya carthayensis fruits, the expression of magnesium-chelatase subunit(CHLH), agnesium-protoporphyrin IX monomethyl ester [oxidative] cyclase(CRD), chlorophyll(ide) b reductase(NYC), light harvesting pigment protein complexes-coding genes(LHCⅡ), light repair protein-coding genes(PSAN, PSAB27, STN7), 38 heat shock proteins(HSP), ribulose bisphosphate carboxylase/oxygenase activase(RCA) and alpha carbonic anhydrase(CA) was significantly up regulated for the pp cross combination. It indicates that the significantly up-regulated expression of genes involved in chlorophyll synthesis, light capture and carbon assimilation might be related to the significantly higher photosynthetic rate in the exocarp of pp cross combination.
【Objective】To elucidate the molecular mechanism for enhancing photosynthetic capacity of the exocarp of Carya carthayensis fruits pollinated by Carya illinoensis in order to provide a theoretic basis for further research on metaxenia.【Method】 Transcriptome sequencing was performed for exocarp of C. cathayensis respectively pollinated by C. cathayensis(marked as hp) and C. illinoensis(marked as pp) with samples collected 65 days after pollination(65DAP) when the fruit rapidly expanding in size. Gene enrichment analysis was conducted for pathways of chlorophyll synthesis, photo-response and carbon assimilation in combination with variation in chlorophyll content, photosynthetic rate and activity of key enzymes involved in the photosynthesis.【Result】Compared to the fruit pollinated with hp, the chlorophyll content, photosynthetic rate, Rubisco activity, and phosphoenolpyruvate carboxylase(PEPC) activity of exocarp in the fruit pollinated with pp were 1.31(P=0.047), 1.12(P=0.000 43), 1.65(P=0.036), and 1.23(P=0.001 3) folds, respectively. A total of 32 908 scaffolds were generated by transcriptome sequencing, and 66 photosynthesis-related genes were screened from 1 894 differentially expressed genes(DEGs)(P <0.05,fold change>1.5), which were mainly involved in pathways of chlorophyll synthesis and photosynthetic carbon fixation. The expression of magnesium-chelatase subunit(CHLH), agnesium-protoporphyrin IX monomethyl ester [oxidative] cyclase(CRD), and chlorophyll(ide) b reductase(NYC) of the fruit pollinated with pp was significantly up-regulated while that of pheophorbide a oxygenase(PAO) was significantly down-regulated in the chlorophyll biosynthesis pathway, and the expression of 16 light harvesting pigment protein complexes(LHCⅡ)-coding genes, ribulose bisphosphate carboxylase/oxygenase activase(RCA), alpha carbonic anhydrase(CA) in the photosynthetic carbon fixation pathway were significantly up-regulated. 42 genes involved in photoprotection of exocarp are also showed significantly high expression in the fruit pollinated with pp than those in the fruit pollinated with hp.【Conclusion】 In the rapid growth period of Carya carthayensis fruits, the expression of magnesium-chelatase subunit(CHLH), agnesium-protoporphyrin IX monomethyl ester [oxidative] cyclase(CRD), chlorophyll(ide) b reductase(NYC), light harvesting pigment protein complexes-coding genes(LHCⅡ), light repair protein-coding genes(PSAN, PSAB27, STN7), 38 heat shock proteins(HSP), ribulose bisphosphate carboxylase/oxygenase activase(RCA) and alpha carbonic anhydrase(CA) was significantly up regulated for the pp cross combination. It indicates that the significantly up-regulated expression of genes involved in chlorophyll synthesis, light capture and carbon assimilation might be related to the significantly higher photosynthetic rate in the exocarp of pp cross combination.
引文
崔喜艳.2008. 基础生物化学实验方法和技术.北京: 中国林业出版社.(Cui X Y. 2008. Basic biochemical experiment methods and techniques. Beijing: China Forestry Publishing House. [in Chinese])
郝再彬, 苍晶, 徐仲. 2004. 植物生理实验. 哈尔滨: 哈尔滨工业大学出版社.(Hao Z B, Cang J, Xu Z. 2004. Plant physiology experiment. Harbin: Harbin Institute of Technology Press. [in Chinese])
洪丹丹. 2007. 山核桃×薄壳山核桃授粉子代AFLP、SSR分析. 杭州: 浙江林学院硕士学位论文.(Hong D D. 2007. AFLP and SSR Analysis of fruit resulting from C. cathayensis×C.cathayensis and C. cathayensis×C. illinoensis. Hangzhou: MS thesis of Zhejiang A & F University. [in Chinese])
孔祥生, 易现峰. 2008. 植物生理学实验技术.北京: 中国农业出版社.(Kong X S, Yi X F. 2018. Experimental techniques for plant physiology. Beijing: China Agriculture Press. [in Chinese])
黎章矩, 夏逍鸿, 施拱生. 1982. 山核桃种间杂交试验研究. 浙江林学院科技通讯,(1).(Li Z J, Xia X H, Shi G S. 1982. Hickory interspecific hybridization experiment research. Science and Technology Communication of Zhejiang Forestry College, (1). [in Chinese])
马婧, 邓楠, 褚建民, 等. 2016. 泡泡刺高通量转录组鉴定及其黄酮类代谢途径初步分析. 林业科学研究, 29(1): 61-66.(Ma J, Deng N, Chu J M, et al. 2016. High-throughput transcriptome identification and flavonoids metabolic pathways in Nitraria sphaerocarpa. Forest Research, 29(1): 61-66. [in Chinese])
施教耐, 吴敏贤, 查静娟. 1979. 植物磷酸烯醇式丙酮酸羧化酶的研究Ⅰ:PEP羧化酶同功酶的分离和变构特性的比较.植物生理学报, (3): 44-54.(Shi J N, Wu M X, Zhai J J. 1979. Study on the phosphate enzymatic acetone carboxylation of plant phosphate-I. Comparison of isolation and allosteric properties of PEP carboxylation. Journal of Plant Physiology, (3): 44-54. [in Chinese])
王玮蔚. 2014. 蛋白核小球藻碳酸酐酶基因筛选及环境因素对其调控的研究. 宁波: 宁波大学硕士学位论文.(Wang W W. 2014. Screening of carbonic anhydrase gene from Chlorella pyrenoidosa and study on its regulation by environmental factors. Ningbo: MS thesis of Ningbo University. [in Chinese])
王正加, 张斌, 夏国华, 等. 2010. 山核桃×薄壳山核桃花粉直感效应与后代分析. 果树学报, 27(6): 908-913.(Wang Z J, Zhang B, Xia G H, et al. 2010. Analysis of the progeny of Carya cathayensis×C. illinoensis and the xenia effect. Journal of Fruit Science, 27(6): 908-913. [in Chinese])
解红恩, 黄有军, 薛霞铭,等. 2008. 山核桃果实生长发育规律. 浙江农林大学学报, 25(4): 527-531.(Xie H E, Huang Y J, Xue X M, et al. 2008. Growth and development of pecan fruit. Journal of Zhejiang A&F University, 25(4): 527-531. [in Chinese])
徐沁怡, 王标, 赵建文,等. 2017. 2种花粉授粉山核桃果皮光合特性的差异比较. 林业科学, 53(1): 38-46.(Xu Q Y, Wang B, Zhao J W, et al. 2017. Variation in photosynthetic characteristics of exocarp of Carya cathayensis fruits pollinated with different pollens. Scientia Silvae Sinicae, 53(1): 38-46. [in Chinese])
叶浩然, 邵慰忠, 常君, 等. 2013.山核桃与薄壳山核桃的杂交优势在山核桃生产中的应用试验. 浙江林业科技, 33(4): 83-85.(Ye H R, Shao W Z, Chang J, et al. 2013. Experiment on artificial pollination of Carya cathayensis by C. illinoensis. Journal of Zhejiang Forestry Science & Technology, 33(4): 83-85. [in Chinese])
叶茂富, 吴厚钧. 1965.山核桃与薄壳山核桃杂交的研究. 林业科学, 10(1): 50-56.(Ye M F, Wu H J. 1965. Study of artificial pollination of Carya cathayensis by C. illinoensis. Scientia Silvae Sinicae, 10(1): 50-56. [in Chinese])
尹吴, 孙伟博, 周燕, 等. 2017. 毛果杨Rubisco活化酶基因的克隆与功能分析. 林业科学, 53(4): 83-95.(Yi W, Sun W B, Zhou Y, et al. 2017. Cloning and functional analysis of Rubisco activase gene from Populus euphratica. Scientia Silvae Sinicae, 53(4): 83-95. [in Chinese])
张斌. 2009. 山核桃雌配子体发育及其生殖过程研究. 杭州: 浙江林学院硕士学位论文.(Zhang B. 2009. Female gametophyte development and reproductive process in gickory(Carya cathayensis). Hangzhou: MS thesis of Zhejiang A & F University. [in Chinese])
张亚杰. 2006. 高等植物光系统Ⅱ大量捕光色素蛋白复合体的稳定性研究. 北京: 中国科学院植物研究所博士学位论文.(Zhang Y J. 2006. Stability of the major light-harvesting complex of photosystem Ⅱ of higher plant. Beijing: PhD thesis of Institute of Botany, The Chinese Academy of Sciences. [in Chinese])
Adamiec M, Gibasiewicz K, Luciński R, et al. 2015. Excitation energy transfer and charge separation are affected in Arabidopsis thaliana mutants lacking light-harvesting chlorophyll a/b binding protein Lhcb3. Journal of Photochemistry & Photobiology B: Biology, 153:423-428.
Aschan G, Pfanz H. 2003. Non-foliar photosynthesis-a strategy of additional carbon acquisition. Flora, 198: 81-97.
Bang W Y, Jeong I S, Kim D W, et al. 2008. Role of Arabidopsis CHL27 protein for photosynthesis, chloroplast development and gene expression profiling. Plant & Cell Physiology, 49(9): 1350-136.
Beale S I. 2005. Green genes gleaned. Trends in Plant Science, 10(7): 309-312.
Birkhold K T, Koch K E, Darnell R L, et al. 1992. Carbon and nitrogen economy of developing rabbiteye blueberry fruit. Journal of the American Society for Horticulturalence, 117(1): 139-145.
Bonardi V, Pesaresi P, Becker T, et al. 2005. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature, 437(7062):1179-1182.
Brown B A, Cloix C, Jiang G H, et al. 2005. A UV-B-specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America, 102(50):18225-18230.
Chen L S, Cheng L. 2003. Carbon assimilation and carbohydrate metabolism of ‘concord’ grape (Vitis labrusca L.) leaves in response to nitrogen supply. Journal of the American Society for Horticultural Science, 128(5): 754-760.
Cocaliadis M F, Fernándezmuňoz R, Pons C, et al. 2014. Increasing tomato fruit quality by enhancing fruit chloroplast function. A double-edged sword?. Journal of Experimental Botany, 65(16): 4589-4598.
Damkjaer J T, Kere?che S, Johnson M P, et al. 2009. The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. The Plant Cell, 21(10): 3245-3256.
Depège N, Bellafiore S, Rochaix J D. 2003. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science, 299(5612): 1572-1575.
Haldrup A, Naver H, Scheller H V. 2010. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem. Plant Journal, 17(6): 689-698.
Hieke S, Menzel C M, Ludders P. 2002. Effects of leaf, shoot and fruit development on photosynthesis of Lychee trees (Litchi chinensis). Tree Physiol, 22(13): 955-961.
Hiratsuka S, Yokoyama Y, Nishimura H, et al. 2012. Fruit photosynthesis and phosphoenolpyruvate carboxylase activity as affected by lightproof fruit bagging in satsuma mandarin. American Society for Horticultural Science, 137(4): 215-220.
Hu Y Y, Zhang Y L, Luo H H, et al. 2012. Important photosynthetic contribution from the non-foliar green organs in cotton at the late growth stage. Planta, 235(2): 325-336.
Hu Y Y, Zhang Y L, Yu W W, et al. 2018. Novel insights into the influence of seed sarcotesta photosynthesis on accumulation of seed dry matter and oil content in Torreya grandis cv. ‘Merrillii’. Frontiers in Plant Sicence, 8: 2179.
Huang H H, Xu L L, Tong Z K, et al. 2012. De novo, characterization of the Chinese fir (Cunninghamia lanceolata) transcriptome and analysis of candidate genes involved in cellulose and lignin biosynthesis. BMC Genomics, 13(1): 648.
Ihalainen J A, Jensen P E, Haldrup A, et al. 2002. Pigment organization and energy transfer dynamics in isolated photosystemⅠ(PSⅠ) complexes from Arabidopsis thaliana depleted of the PSⅠ-G, PSⅠ-K, PSⅠ-L, or PSⅠ-N subunit. Biophysical Journal, 83(4): 2190-2201.
Ito H, Tanaka A. 2014. Evolution of a new chlorophyll metabolic pathway driven by the dynamic changes in enzyme promiscuous activity. Plant & Cell Physiology, 55(3):593-603.
Li S W, Shi R F, Leng Y. 2015. De novo characterization of the mung bean transcriptome and transcriptomic analysis of adventitious rooting in seedlings using RNA-Seq. PLoS One, 10(7): e0132969.
Li X, Hou J, Bai K, et al. 2004. Activity and distribution of carbonic anhydrase in leaf and ear parts of wheat (Triticum aestivum L.). Plant Science, 166(3): 627-632.
Li X J, Wang H G, Li H B, et al. 2006. Awns play a dominant role in carbohydrate production during the grain-filling stages in wheat (Triticum aestivum). Physiologia Plantarum, 127: 701-709.
Lichtenthaler H K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol, 148 (1):350-382.
Lin Q, Wang C, Dong W, et al. 2015. Transcriptome and metabolome analyses of sugar and organic acid metabolism in Ponkan (Citrus reticulata) fruit during fruit maturation. Gene, 554(1):64-74.
Makino A, Mae T, Ohira K. 1983. Photosynthesis and ribulose 1,5-bisphosphate carboxylase in rice leaves: changes in photosynthesis and enzymes involved in carbon assimilation from leaf development through senescence. Plant Physiology, 73(4):1002-1007.
Meng L, Fan Z, Zhang Q, et al. 2018. BEL1-LIKE HOMEODOMAIN 11 regulates chloroplast development and chlorophyll synthesis in tomato fruit. Plant Journal for Cell & Molecular Biology, 94(6):1126-1140.
Nowaczyk M M, Hebeler R, Schlodder E, et al. 2006. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem Ⅱ. Plant Cell, 18(11):3121-3131.
Pavel E W, Dejong T M. 2010. Estimating the photosynthetic contribution of developing peach (Prunus persica) fruits to their growth and maintenance carbohydrate requirements. Physiologia Plantarum, 88(2): 331-338.
Pesaresi P, Hertle A, Pribil M, et al. 2009. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell, 21(8): 2402-2423.
Poong S W, Lee K K, Lim P E, et al. 2018. RNA-Seq-mediated transcriptomic analysis of heat stress response in a polar Chlorella sp. (Trebouxiophyceae, Chlorophyta). Journal of Applied Phycology, doi:10.1007/s10811-018-1455-9.
Portis R. 1995. The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany, 46: 1285-1291.
Salvucci M E, Ogren W L. 1996. The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. Photosynthesis Research, 47(1):1-11.
Sawers R J, Viney J, Farmer P R, et al. 2006. The maize oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Mol Biol, 60(1): 95-106.
Schuster G, Timberg R, Ohad I. 1988. Turnover of thylakoid photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Febs Journal, 177(2):403-410.
Waters E R. 1995. The molecular evolution of the small heat-shock proteins in plants. Genetics, 141(2):785-795.
Wu Z, Zhang X, He B, et al. 2007. A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiology, 145(1): 29-40.
Xu Q, Wu J, Cao Y, et al. 2016. Photosynthetic characteristics of leaves and fruits of Hickory (Carya cathayensis Sarg.) and Pecan (Carya illinoensis K. Koch) during fruit development stages. Trees, 30(5):1-12.
郝再彬, 苍晶, 徐仲. 2004. 植物生理实验. 哈尔滨: 哈尔滨工业大学出版社.(Hao Z B, Cang J, Xu Z. 2004. Plant physiology experiment. Harbin: Harbin Institute of Technology Press. [in Chinese])
洪丹丹. 2007. 山核桃×薄壳山核桃授粉子代AFLP、SSR分析. 杭州: 浙江林学院硕士学位论文.(Hong D D. 2007. AFLP and SSR Analysis of fruit resulting from C. cathayensis×C.cathayensis and C. cathayensis×C. illinoensis. Hangzhou: MS thesis of Zhejiang A & F University. [in Chinese])
孔祥生, 易现峰. 2008. 植物生理学实验技术.北京: 中国农业出版社.(Kong X S, Yi X F. 2018. Experimental techniques for plant physiology. Beijing: China Agriculture Press. [in Chinese])
黎章矩, 夏逍鸿, 施拱生. 1982. 山核桃种间杂交试验研究. 浙江林学院科技通讯,(1).(Li Z J, Xia X H, Shi G S. 1982. Hickory interspecific hybridization experiment research. Science and Technology Communication of Zhejiang Forestry College, (1). [in Chinese])
马婧, 邓楠, 褚建民, 等. 2016. 泡泡刺高通量转录组鉴定及其黄酮类代谢途径初步分析. 林业科学研究, 29(1): 61-66.(Ma J, Deng N, Chu J M, et al. 2016. High-throughput transcriptome identification and flavonoids metabolic pathways in Nitraria sphaerocarpa. Forest Research, 29(1): 61-66. [in Chinese])
施教耐, 吴敏贤, 查静娟. 1979. 植物磷酸烯醇式丙酮酸羧化酶的研究Ⅰ:PEP羧化酶同功酶的分离和变构特性的比较.植物生理学报, (3): 44-54.(Shi J N, Wu M X, Zhai J J. 1979. Study on the phosphate enzymatic acetone carboxylation of plant phosphate-I. Comparison of isolation and allosteric properties of PEP carboxylation. Journal of Plant Physiology, (3): 44-54. [in Chinese])
王玮蔚. 2014. 蛋白核小球藻碳酸酐酶基因筛选及环境因素对其调控的研究. 宁波: 宁波大学硕士学位论文.(Wang W W. 2014. Screening of carbonic anhydrase gene from Chlorella pyrenoidosa and study on its regulation by environmental factors. Ningbo: MS thesis of Ningbo University. [in Chinese])
王正加, 张斌, 夏国华, 等. 2010. 山核桃×薄壳山核桃花粉直感效应与后代分析. 果树学报, 27(6): 908-913.(Wang Z J, Zhang B, Xia G H, et al. 2010. Analysis of the progeny of Carya cathayensis×C. illinoensis and the xenia effect. Journal of Fruit Science, 27(6): 908-913. [in Chinese])
解红恩, 黄有军, 薛霞铭,等. 2008. 山核桃果实生长发育规律. 浙江农林大学学报, 25(4): 527-531.(Xie H E, Huang Y J, Xue X M, et al. 2008. Growth and development of pecan fruit. Journal of Zhejiang A&F University, 25(4): 527-531. [in Chinese])
徐沁怡, 王标, 赵建文,等. 2017. 2种花粉授粉山核桃果皮光合特性的差异比较. 林业科学, 53(1): 38-46.(Xu Q Y, Wang B, Zhao J W, et al. 2017. Variation in photosynthetic characteristics of exocarp of Carya cathayensis fruits pollinated with different pollens. Scientia Silvae Sinicae, 53(1): 38-46. [in Chinese])
叶浩然, 邵慰忠, 常君, 等. 2013.山核桃与薄壳山核桃的杂交优势在山核桃生产中的应用试验. 浙江林业科技, 33(4): 83-85.(Ye H R, Shao W Z, Chang J, et al. 2013. Experiment on artificial pollination of Carya cathayensis by C. illinoensis. Journal of Zhejiang Forestry Science & Technology, 33(4): 83-85. [in Chinese])
叶茂富, 吴厚钧. 1965.山核桃与薄壳山核桃杂交的研究. 林业科学, 10(1): 50-56.(Ye M F, Wu H J. 1965. Study of artificial pollination of Carya cathayensis by C. illinoensis. Scientia Silvae Sinicae, 10(1): 50-56. [in Chinese])
尹吴, 孙伟博, 周燕, 等. 2017. 毛果杨Rubisco活化酶基因的克隆与功能分析. 林业科学, 53(4): 83-95.(Yi W, Sun W B, Zhou Y, et al. 2017. Cloning and functional analysis of Rubisco activase gene from Populus euphratica. Scientia Silvae Sinicae, 53(4): 83-95. [in Chinese])
张斌. 2009. 山核桃雌配子体发育及其生殖过程研究. 杭州: 浙江林学院硕士学位论文.(Zhang B. 2009. Female gametophyte development and reproductive process in gickory(Carya cathayensis). Hangzhou: MS thesis of Zhejiang A & F University. [in Chinese])
张亚杰. 2006. 高等植物光系统Ⅱ大量捕光色素蛋白复合体的稳定性研究. 北京: 中国科学院植物研究所博士学位论文.(Zhang Y J. 2006. Stability of the major light-harvesting complex of photosystem Ⅱ of higher plant. Beijing: PhD thesis of Institute of Botany, The Chinese Academy of Sciences. [in Chinese])
Adamiec M, Gibasiewicz K, Luciński R, et al. 2015. Excitation energy transfer and charge separation are affected in Arabidopsis thaliana mutants lacking light-harvesting chlorophyll a/b binding protein Lhcb3. Journal of Photochemistry & Photobiology B: Biology, 153:423-428.
Aschan G, Pfanz H. 2003. Non-foliar photosynthesis-a strategy of additional carbon acquisition. Flora, 198: 81-97.
Bang W Y, Jeong I S, Kim D W, et al. 2008. Role of Arabidopsis CHL27 protein for photosynthesis, chloroplast development and gene expression profiling. Plant & Cell Physiology, 49(9): 1350-136.
Beale S I. 2005. Green genes gleaned. Trends in Plant Science, 10(7): 309-312.
Birkhold K T, Koch K E, Darnell R L, et al. 1992. Carbon and nitrogen economy of developing rabbiteye blueberry fruit. Journal of the American Society for Horticulturalence, 117(1): 139-145.
Bonardi V, Pesaresi P, Becker T, et al. 2005. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature, 437(7062):1179-1182.
Brown B A, Cloix C, Jiang G H, et al. 2005. A UV-B-specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America, 102(50):18225-18230.
Chen L S, Cheng L. 2003. Carbon assimilation and carbohydrate metabolism of ‘concord’ grape (Vitis labrusca L.) leaves in response to nitrogen supply. Journal of the American Society for Horticultural Science, 128(5): 754-760.
Cocaliadis M F, Fernándezmuňoz R, Pons C, et al. 2014. Increasing tomato fruit quality by enhancing fruit chloroplast function. A double-edged sword?. Journal of Experimental Botany, 65(16): 4589-4598.
Damkjaer J T, Kere?che S, Johnson M P, et al. 2009. The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. The Plant Cell, 21(10): 3245-3256.
Depège N, Bellafiore S, Rochaix J D. 2003. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science, 299(5612): 1572-1575.
Haldrup A, Naver H, Scheller H V. 2010. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem. Plant Journal, 17(6): 689-698.
Hieke S, Menzel C M, Ludders P. 2002. Effects of leaf, shoot and fruit development on photosynthesis of Lychee trees (Litchi chinensis). Tree Physiol, 22(13): 955-961.
Hiratsuka S, Yokoyama Y, Nishimura H, et al. 2012. Fruit photosynthesis and phosphoenolpyruvate carboxylase activity as affected by lightproof fruit bagging in satsuma mandarin. American Society for Horticultural Science, 137(4): 215-220.
Hu Y Y, Zhang Y L, Luo H H, et al. 2012. Important photosynthetic contribution from the non-foliar green organs in cotton at the late growth stage. Planta, 235(2): 325-336.
Hu Y Y, Zhang Y L, Yu W W, et al. 2018. Novel insights into the influence of seed sarcotesta photosynthesis on accumulation of seed dry matter and oil content in Torreya grandis cv. ‘Merrillii’. Frontiers in Plant Sicence, 8: 2179.
Huang H H, Xu L L, Tong Z K, et al. 2012. De novo, characterization of the Chinese fir (Cunninghamia lanceolata) transcriptome and analysis of candidate genes involved in cellulose and lignin biosynthesis. BMC Genomics, 13(1): 648.
Ihalainen J A, Jensen P E, Haldrup A, et al. 2002. Pigment organization and energy transfer dynamics in isolated photosystemⅠ(PSⅠ) complexes from Arabidopsis thaliana depleted of the PSⅠ-G, PSⅠ-K, PSⅠ-L, or PSⅠ-N subunit. Biophysical Journal, 83(4): 2190-2201.
Ito H, Tanaka A. 2014. Evolution of a new chlorophyll metabolic pathway driven by the dynamic changes in enzyme promiscuous activity. Plant & Cell Physiology, 55(3):593-603.
Li S W, Shi R F, Leng Y. 2015. De novo characterization of the mung bean transcriptome and transcriptomic analysis of adventitious rooting in seedlings using RNA-Seq. PLoS One, 10(7): e0132969.
Li X, Hou J, Bai K, et al. 2004. Activity and distribution of carbonic anhydrase in leaf and ear parts of wheat (Triticum aestivum L.). Plant Science, 166(3): 627-632.
Li X J, Wang H G, Li H B, et al. 2006. Awns play a dominant role in carbohydrate production during the grain-filling stages in wheat (Triticum aestivum). Physiologia Plantarum, 127: 701-709.
Lichtenthaler H K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol, 148 (1):350-382.
Lin Q, Wang C, Dong W, et al. 2015. Transcriptome and metabolome analyses of sugar and organic acid metabolism in Ponkan (Citrus reticulata) fruit during fruit maturation. Gene, 554(1):64-74.
Makino A, Mae T, Ohira K. 1983. Photosynthesis and ribulose 1,5-bisphosphate carboxylase in rice leaves: changes in photosynthesis and enzymes involved in carbon assimilation from leaf development through senescence. Plant Physiology, 73(4):1002-1007.
Meng L, Fan Z, Zhang Q, et al. 2018. BEL1-LIKE HOMEODOMAIN 11 regulates chloroplast development and chlorophyll synthesis in tomato fruit. Plant Journal for Cell & Molecular Biology, 94(6):1126-1140.
Nowaczyk M M, Hebeler R, Schlodder E, et al. 2006. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem Ⅱ. Plant Cell, 18(11):3121-3131.
Pavel E W, Dejong T M. 2010. Estimating the photosynthetic contribution of developing peach (Prunus persica) fruits to their growth and maintenance carbohydrate requirements. Physiologia Plantarum, 88(2): 331-338.
Pesaresi P, Hertle A, Pribil M, et al. 2009. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell, 21(8): 2402-2423.
Poong S W, Lee K K, Lim P E, et al. 2018. RNA-Seq-mediated transcriptomic analysis of heat stress response in a polar Chlorella sp. (Trebouxiophyceae, Chlorophyta). Journal of Applied Phycology, doi:10.1007/s10811-018-1455-9.
Portis R. 1995. The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany, 46: 1285-1291.
Salvucci M E, Ogren W L. 1996. The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. Photosynthesis Research, 47(1):1-11.
Sawers R J, Viney J, Farmer P R, et al. 2006. The maize oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Mol Biol, 60(1): 95-106.
Schuster G, Timberg R, Ohad I. 1988. Turnover of thylakoid photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Febs Journal, 177(2):403-410.
Waters E R. 1995. The molecular evolution of the small heat-shock proteins in plants. Genetics, 141(2):785-795.
Wu Z, Zhang X, He B, et al. 2007. A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiology, 145(1): 29-40.
Xu Q, Wu J, Cao Y, et al. 2016. Photosynthetic characteristics of leaves and fruits of Hickory (Carya cathayensis Sarg.) and Pecan (Carya illinoensis K. Koch) during fruit development stages. Trees, 30(5):1-12.