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Journal of Integrative Agriculture  2024, Vol. 23 Issue (02): 590-604    DOI: 10.1016/j.jia.2023.04.011
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The evolution and diurnal expression patterns of photosynthetic pathway genes of the invasive alien weed, Mikania micrantha

Kangkang Wang1, 2, 3, Mengjiao Jin1, Jingjing Li1, 2, 3, Yesong Ren1, Zaiyuan Li1, Xinghai Ren1, Cong Huang1, Fanghao Wan1#, Wanqiang Qian1#, Bo Liu1#

1 Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture/Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China

2 State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China

3 Shenzhen Research Institute of Henan University, Shenzhen 518000, China

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摘要  

薇甘菊(Mikania micrantha)是一种快速生长的全球性入侵杂草,广泛分布在热带和亚热带地区。薇甘菊的入侵会对当地自然生态系统造成严重破坏,并对森林和作物生产造成巨大的经济损失。它在光合作用方面具有优势,其净光合速率与C4植物相近,固碳能力较高。研究表明薇甘菊的光合能力是其快速生长和快速殖民新栖息地的重要原因之一。然而,目前尚没有研究揭示薇甘菊光合作用的进化机制和昼夜规律。本研究采用基因组学和转录组学相结合的方法,揭示了薇甘菊光合作用的进化机制和昼夜表达模式。结果显示,在薇甘菊中有16个正选择基因,主要集中于光反应和光同化物的利用两个过程中,并且叶绿素a/b结合蛋白、苹果酸脱氢酶、丙酮酸正磷酸二激酶和苹果酸酶家族的基因数量与C4植物(高粱或玉米)相似,显著高于其他植物。在不同组织中,98.1%与光反应相关的基因在茎中具有较高表达,C4循环相关的基因中有一半以上在茎中高于叶中的表达。气孔开闭过程中,2个碳酸酐酶基因在18:00的表达量高于8:00SLAC1HT1基因在18:00表达量最低。此外,与光合作用相关的基因在7:0017:00表达量较高。因此我们推测,薇甘菊能够在茎和花器官中进行光合作用,并且叶片的一些气孔在夜间能够通过CO2信号打开。此外,它的进化可能会减弱高光强时的光抑制,并在低光强时提高光合作用的效率。组织特异性光合类型和光合相关基因的不同昼夜模式可能有助于薇甘菊在新栖息地的快速定植。薇甘菊可能通过这些变化增加了它的种间优势和侵袭性。本文的研究结果为了解薇甘菊的光合作用机制及其控制和生物利用度提供了有价值的信息。



Abstract  

Mikania micrantha is a fast-growing global invasive weed species that causes severe damage to natural ecosystems and very large economic losses of forest and crop production.  It has advantages in photosynthesis, including a similar net photosynthetic rate as C4 plants and a higher carbon fixation capacity.  We used a combination of genomics and transcriptomics approaches to study the evolutionary mechanisms and circadian expression patterns of Mmicrantha.  In Mmicrantha, 16 positive selection genes focused on photoreaction and utilization of photoassimilates.  In different tissues, 98.1% of the genes associated with photoresponse had high expression in stems, and more than half of the genes of the C4 cycle had higher expression in stems than in leaves.  In stomatal opening and closing, 2 genes of carbonic anhydrase (CAs) had higher expression at 18:00 than at 8:00, and the slow anion channel 1 (SLAC1) and high-leaf-temperature 1 kinase (HT1) genes were expressed at low levels at 18:00.  In addition, genes associated with photosynthesis had higher expression levels at 7:00 and 17:00.  We hypothesized that Mmicrantha may undergo photosynthesis in the stem and flower organs and that some stomata of the leaves were opening at night by CO2 signals.  In addition, its evolution may attenuate photoinhibition at high light intensities, and enhance more efficient of photosynthesis during low light intensity.  And the tissue-specific photosynthetic types and different diurnal pattern of photosynthetic-related genes may contribute to its rapid colonization of new habitats of Mmicrantha.

Keywords:  invasion plant        Mikania micrantha        photosynthesis        stomata        stem   
Received: 30 December 2022   Accepted: 03 March 2023
Fund: 

The work was funded by the National Natural Science Foundation of China (32072490), the National Key R&D Program of China (2021YFC2600100 and 2021YFC2600101), and the Agricultural Science and Technology Innovation Program, China.

About author:  Kangkang Wang, E-mail: 18351212377@163.com; #Correspondence Bo Liu, E-mail: liubo03@caas.cn; Wanqiang Qian, E-mail: qianwanqiang@caas.cn; Fanghao Wan, E-mail: wanfanghao@caas.cn

Cite this article: 

WANG Kang-kang, JIN Meng-jiao, LI Jing-jing, REN Ye-song, LI Zai-yuan, REN Xing-hai, HUANG Cong, WAN Fang-hao, QIAN Wan-qiang, LIU Bo. 2024.

The evolution and diurnal expression patterns of photosynthetic pathway genes of the invasive alien weed, Mikania micrantha . Journal of Integrative Agriculture, 23(02): 590-604.

Ainsworth E A. 2018. Photosynthesis. In: Hatfield J L, Sivakumar M V K, Prueger J H, eds., Agroclimatology. Wiley, Madison, USA. pp. 129–151.

Anders S, Pyl P T, Huber W. 2015. HTSeq - A python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166–169.

Ávila E, Herrera A, Tezara W. 2014. Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica, 52, 3–15.

Ávila-Lovera E, Garcillán P P. 2021. Phylogenetic signal and climatic niche of stem photosynthesis in the mediterranean and desert regions of California and Baja California Peninsula. American Journal of Botany, 108, 334–345.

Ávila-Lovera E, Zerpa A J, Santiago L S. 2017. Stem photosynthesis and hydraulics are coordinated in desert plant species. New Phytologist, 216, 1119–1129.

Brown N J, Palmer B G, Stanley S, Hajaji H, Janacek S H, Astley H M, Parsley K, Kajala K, Quick W P, Trenkamp S, Fernie A R, Maurino V G, Hibberd J M. 2010. C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. The Plant Journal, 61, 122–133.

Chang Y C, Walling L L. 1992. Chlorophyll a/b-binding protein genes are differentially expressed during soybean development. Plant Molecular Biology, 19, 217–230.

Dann M, Leister D. 2017. Enhancing (crop) plant photosynthesis by introducing novel genetic diversity. Philosophical Transactions of the Royal Society, 372, 20160380.

Day M D, Clements D R, Gile C, Senaratne W K A D, Shen S, Weston L A, Zhang F. 2016. Biology and Impacts of Pacific Islands Invasive Species. 13. Mikania micrantha Kunth (Asteraceae). Pacific Science, 70, 257–285.

Deng X. 2010. Morphological and physiological plasticity responding to different light environments of the invasive plant, Mikania micrantha H.B.Kunth. Ecology and Environment, 19, 1170–1175. (in Chinese)

Deng Y, Kashtoh H, Wang Q, Zhen G, Li Q, Tang L, Gao H, Zhang C, Qin L, Su M, Li F, Huang X, Wang Y, Xie Q, Clarke O B, Hendrickson W A, Chen Y. 2021. Structure and activity of SLAC1 channels for stomatal signaling in leaves. Proceedings of the National Academy of Sciences of the United States of America, 118, e2015151118.

Edgar R C. 2004. MUSCLE, multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

Ehleringer J, Pearcy R W. 1983. Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiology, 73, 555–559.

Emms D M, Kelly S. 2015. OrthoFinder, solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology, 16, 157.

Fariduddin Q, Hayat S, Ali B, Ahmad A. 2006. Effect of 28-homobrassinolide on the nitrate reductase, carbonic anhydrase activities and net photosynthetic rate in Vigna radiata. Acta Botanica Croatica, 65, 19–23.

Fracheboud Y. 2002. Identification of quantitative trait loci for cold-tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany, 53, 1967–1977.

Gombos Z, Wada H, Murata N. 1994. The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids, a mechanism of chilling tolerance. Proceedings of the National Academy of Sciences of the United States of America, 91, 8787–8791.

Goulard F, Lüning K, Jacobsen S. 2004. Circadian rhythm of photosynthesis and concurrent oscillations of transcript abundance of photosynthetic genes in the marine red alga Grateloupia turuturu. European Journal of Phycology, 39, 431–437.

Guo W, Liu Y, Ng W L, Liao P C, Huang B H, Li W, Li C, Shi X, Huang Y. 2018. Comparative transcriptome analysis of the invasive weed Mikania micrantha with its native congeners provides insights into genetic basis underlying successful invasion. BMC Genomics, 19, 392.

Hasegawa K, Yukawa Y, Sugita M, Sugiura M. 2002. Organization and transcription of the gene family encoding chlorophyll a/b-binding proteins in Nicotiana sylvestris. Gene, 289, 161–168.

Hashimoto M, Negi J, Young J, Israelsson M, Schroeder J I, Iba K. 2006. Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nature Cell Biology, 8, 391–397.

Heyduk K, Moreno-Villena J J, Gilman I S, Christin P A, Edwards E J. 2019. The genetics of convergent evolution, insights from plant photosynthesis. Nature Reviews Genetics, 20, 485–493.

Hibberd J M, Quick W P. 2002. Characteristics of C4 photosynthesis in stems and petioles of C3 owering plants. Nature, 415, 451–454.

Hiratsuka S, Suzuki M, Nishimura H, Nada K. 2015. Fruit photosynthesis in Satsuma mandarin. Plant Science, 241, 65–69.

Hu S P, Zhou Y, Zhang L, Zhu X D, Li L, Luo L J, Liu G L, Zhou Q M. 2009. Correlation and quantitative trait loci analyses of total chlorophyll content and photosynthetic rate of rice (Oryza sativa) under water stress and well-watered Conditions. Journal of Integrative Plant Biology, 51, 879–888.

Hussain A, Nazir F, Fariduddin Q. 2019. 24-Epibrassinolide and spermidine alleviate Mn stress via the modulation of root morphology, stomatal behavior, photosynthetic attributes and antioxidant defense in Brassica juncea. Physiology and Molecular Biology of Plants, 25, 905–919.

Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M. 2003. Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 100, 4921–4926.

Jung H S, Niyogi K K. 2009. Quantitative genetic analysis of thermal dissipation in Arabidopsis. Plant Physiology, 150, 977–986.

Keren N, Ohad I. 1998. State transition and photoinhibition. In: Advances in Photosynthesis and Respiration. Springer, Dordrecht. pp. 569–596.

Keren N, Ohkawa H, Welsh E A, Liberton M, Pakrasi H B. 2005. Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell, 17, 2768–2781.

Kim D, Paggi J M, Park C, Bennett C, Salzberg S L. 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907–915.

Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K. 2001. Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature, 414, 656–660.

Kitaya Y, Yabuki K, Kiyota M, Tani A, Hirano T, Aiga I. 2002. Gas exchange and oxygen concentration in pneumatophores and prop roots of four mangrove species. Trees, 16, 155–158.

Koyama K, Kikuzawa K. 2009. Is whole-plant photosynthetic rate proportional to leaf area? A test of scalings and a logistic equation by leaf demography census. American Naturalist, 5, 640–649.

Kusumi K, Hashimura A, Yamamoto Y, Negi J, Iba K. 2017. Contribution of the S-type anion channel SLAC1 to stomatal control and its dependence on developmental stage in rice. Plant and Cell Physiology, 58, 2085–2094.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/Map format and SAMtools. Bioinformatics, 25, 2078–2079.

Li H, Tong Y, Li B, Jing R, Lu C, Li Z. 2010. Genetic analysis of tolerance to photo-oxidative stress induced by high light in winter wheat (Triticum aestivum L.). Journal of Genetics and Genomics, 37, 399–412.

Liu B, Yan J, Li W, Yin L, Li P, Yu H, Xing L, Cai M, Wang H, Zhao M, Zheng J, Sun F, Wang Z, Jiang Z, Ou Q, Li S, Qu L, Zhang Q, Zheng Y, Qiao X, et al. 2020. Mikania micrantha genome provides insights into the molecular mechanism of rapid growth. Nature Communications, 11, 340.

Locke A M, Slattery R A, Ort D R. 2018. Field‐grown soybean transcriptome shows diurnal patterns in photosynthesis‐related processes. Plant Direct, 2, e00099.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Lowe S, Browne M, Boudjelas S, Poorter M. 2000. 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. The International Union for Conservation of Nature (IUCN)/The Species Survival Commission (SSC), Auckland. p. 12.

Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064–1068.

Macanawai A R, Day M D, Tumaneng-Diete T, Adkins S W. 2012. Impact of Mikania micrantha on crop production systems in Viti Levu, Fiji. Pakistan Journal of Weed Science Research, 18, 357–365.

Mallmann J, Heckmann D, Bräutigam A, Lercher M J, Weber A P, Westhoff P, Gowik U. 2014. The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife, 3, e02478.

Martino-Catt S, Ort D R. 1992. Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proceedings of the National Academy of Sciences of the United States of America, 89, 3731–3735.

Matrosova A, Bogireddi H, Mateo-Peñas A, Hashimoto-Sugimoto M, Iba K, Schroeder J I, Israelsson-Nordström M. 2015. The HT1 protein kinase is essential for red light-induced stomatal opening and genetically interacts with OST1 in red light and CO2-induced stomatal movement responses. New Phytologist, 208, 1126–1137.

Meyer H, Thienel U, Piechulla B. 1989. Molecular characterization of the diurnal/circadian expression of the chlorophyll a/b-binding proteins in leaves of tomato and other dicotyledonous and monocotyledonous plant species. Planta, 180, 5–15.

Murata N, Nishiyama Y. 2018. ATP is a driving force in the repair of photosystem II during photoinhibition. Plant, Cell and Environment, 41, 285–299.

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev S I. 2007. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta, 1767, 414–421.

Mustilli A C, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell, 14, 3089–3099.

Nakahira Y, Baba K, Yoneda A, Shiina T, Toyoshima Y. 1998. Circadian-regulated transcription of the psbD light-responsive promoter in wheat chloroplasts. Plant Physiology, 118, 1079–1088.

Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K. 2008. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature, 452, 483–486.

Noordally Z B, Ishii K, Atkins K A, Wetherill S J, Kusakina J, Walton E J, Kato, M, Azuma M, Tanaka K, Hanaoka M, Dodd A N. 2013. Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science, 6125, 1316–1319.

Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T F, Alfred S E, Bonetta D, Finkelstein R, Provart N J, Desveaux D, Rodriguez P L, McCourt P, Zhu J K, Schroeder J I, Volkman B F, et al. 2009. Abscisic acid inhibits PP2Cs via the PYR/PYL family of ABA-binding START proteins. Science, 324, 1068–1071.

Perchorowicz J T, Raynes D A, Jensen R G. 1981. Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proceedings of the National Academy of Sciences of the United States of America, 78, 2985–2989.

Rangan P, Wankhede D P, Subramani R, Chinnusamy V, Malik S K, Baig M J, Singh K, Henry R. 2022. Evolution of an intermediate C4 photosynthesis in the non-foliar tissues of the Poaceae. Photosynthesis Research, 153, 125–134.

Roelfsema M R G, Hanstein S, Felle H H, Hedrich R. 2002. CO2 provides an intermediate link in the red light response of guard cells. Plant Journal, 32, 65–75.

Romanowska E, Powikrowska M, Zienkiewicz M, Pokorska B. 2008. High light induced accumulation of two isoforms of the CF1 α-subunit in mesophyll and bundle sheath chloroplasts of C4 plants. Acta Biochimica Polonica, 55, 175–182.

Sakoda K, Yamori W, Groszmann M, Evans J R. 2021. Stomatal, mesophyll conductance, and biochemical limitations to photosynthesis during induction. Plant Physiology, 185, 146–160.

Skillman J B. 2008. Quantum yield variation across the three pathways of photosynthesis, not yet out of the dark. Journal of Experimental Botany, 59, 1647–1661.

Sun W, Ma N, Huang H, Wei J, Ma S, Liu H, Zhang S, Zhang Z, Sui X, Li X. 2021. Photosynthetic contribution and characteristics of cucumber stems and petioles. BMC Plant Biology, 21, 454.

Suyama M, Torrents D, Bork P. 2006. PAL2NAL, robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34, W609–W612.

von Sydow L, Schwenkert S, Meurer J, Funk C, Mamedov F, Schröder W P. 2016. The PsbY protein of Arabidopsis Photosystem II is important for the redox control of cytochrome b559. Biochimica et Biophysica Acta, 1857, 1524–1533.

Tinoco-Ojanguren C. 2008. Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. Journal of Arid Environments, 72, 127–140.

Tullberg A, Alexciev K, Pfannschmidt T, Allen J F. 2000. Photosynthetic electron flow regulates transcription of the psaB gene in pea (Pisum sativum L.) chloroplasts through the redox state of the plastoquinone pool. Plant and Cell Physiology, 41, 1045–1054.

Tyystjärvi E, Aro E M. 1996. The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proceedings of the National Academy of Sciences of the United States of America, 93, 2213–2218.

Ueno O, Fuchikami Y. 2020. Structure and photosynthetic metabolism in green prop roots of C4 sorghum. Plant Production Science, 23, 182–190.

Wang F, Sun H, Rong L, Li Z, An T, Hu W, Ye Z. 2021. Genotypic-dependent alternation in D1 protein turnover and PSII repair cycle in psf mutant rice (Oryza sativa L.), as well as its relation to light-induced leaf senescence. Plant Growth Regulation, 95, 121–136.

Wasilewska-Dębowska W, Zienkiewicz M, Drozak A. 2022. How light reactions of photosynthesis in C4 plants are optimized and protected under high light conditions. International Journal of Molecular Sciences, 23, 3626.

Watillon B, Kettmann R, Boxus P, Burny A. 1993. Developmental and circadian pattern of rubisco activase mRNA accumulation in apple plants. Plant Molecular Biology, 23, 501–509.

Wen D, Ye W, Feng H, Cai C. 2000. Comparison of basic photosynthetic characteristics between exotic invader weed Mikania micrantha and its companion species. Journal of Tropical and Subtropical Botany, 8, 139–146.

Xu D H, Fang X W, Su P X, Wang G. 2012. Ecophysiological responses of Caragana korshinskii Kom. under extreme drought stress, Leaf abscission and stem survives. Photosynthetica, 50, 541–548.

Yamori W, Evans J R, Von Caemmerer S. 2010. Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation rate in tobacco leaves. Plant, Cell and Environment, 33, 332–343.

Yang Z. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22, 1107–1118.

Yang Z. 2007. PAML 4, phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586–1591.

Zhang N, Kallis R P, Ewy R G, Portis A R. 2002. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proceedings of the National Academy of Sciences of the United States of America, 99, 3330–3334.

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