Acceleration of Carbon Fixation in Chilling-Sensitive Banana under Mild and Moderate Chilling Stresses

. 2020 Dec 07 ; 21 (23) : . [epub] 20201207

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33297477

Grantová podpora
2018YFD1000300 National Key Research and Development Program of China
2018B020202005 the Key Research and Development Program of Guangdong Province for Modern Plant Breeding
2020KJ109 the Guangdong Province Special Fund for Modern Agriculture Industry Technology Innovation Teams
CARS-31-04 the Earmarked Fund for Modern Agro-industry Technology Research System
CZ.02.1.01/0.0/16_019/0000827 the European Regional Development Fund (ERDF) for the project "Plants as a tool for sustainable development"

Banana is one of the most important food and fruit crops in the world and its growth is ceasing at 10-17 °C. However, the mechanisms determining the tolerance of banana to mild (>15 °C) and moderate chilling (10-15 °C) are elusive. Furthermore, the biochemical controls over the photosynthesis in tropical plant species at low temperatures above 10 °C is not well understood. The purpose of this research was to reveal the response of chilling-sensitive banana to mild (16 °C) and moderate chilling stress (10 °C) at the molecular (transcripts, proteins) and physiological levels. The results showed different transcriptome responses between mild and moderate chilling stresses, especially in pathways of plant hormone signal transduction, ABC transporters, ubiquinone, and other terpenoid-quinone biosynthesis. Interestingly, functions related to carbon fixation were assigned preferentially to upregulated genes/proteins, while photosynthesis and photosynthesis-antenna proteins were downregulated at 10 °C, as revealed by both digital gene expression and proteomic analysis. These results were confirmed by qPCR and immunofluorescence labeling methods. Conclusion: Banana responded to the mild chilling stress dramatically at the molecular level. To compensate for the decreased photosynthesis efficiency caused by mild and moderate chilling stresses, banana accelerated its carbon fixation, mainly through upregulation of phosphoenolpyruvate carboxylases.

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Chinnusamy V., Zhu J., Zhu J.K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12:444–451. doi: 10.1016/j.tplants.2007.07.002. PubMed DOI

Hussain H.A., Hussain S., Khaliq A., Ashraf U., Anjum S.A., Men S.N., Wang L.C. Chilling and drought stresses in crop plants: Implications, cross talk, and potential management opportunities. Front. Plant Sci. 2018;9:393. doi: 10.3389/fpls.2018.00393. PubMed DOI PMC

Yang Q.S., Gao J., He W.D., Dou T.X., Ding L.J., Wu J.H., Li C.Y., Peng X.X., Zhang S., Yi G.J. Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress. BMC Genom. 2015;16:446. doi: 10.1186/s12864-015-1551-z. PubMed DOI PMC

Chen C.J., Zhang Y.F., Xu Z.Q., Luan A.P., Mao Q., Feng J.J., Xie T., Gong X., Wang X.S., Chen X., et al. Transcriptome profiling of the pineapple under low temperature to facilitate its breeding for cold tolerance. PLoS ONE. 2016;11:e0163315. doi: 10.1371/journal.pone.0163315. PubMed DOI PMC

Wang J.S., Zhang Q., Cui F., Hou L., Zhao S.Z., Xia H., Qiu J.J., Li T.T., Zhang Y., Wang X.J., et al. Genome-wide analysis of gene expression provides new insights into cold responses in Thellungiella salsuginea. Front. Plant Sci. 2017;8:713. doi: 10.3389/fpls.2017.00713. PubMed DOI PMC

Guo H., Wu T.K., Li S.H., He Q., Deng H.F. The methylation patterns and transcriptional responses to chilling stress at the seedling stage in rice. Int. J. Mol. Sci. 2019;20:5089. doi: 10.3390/ijms20205089. PubMed DOI PMC

Yu X.L., Li Y.H., He C., Zhou J.T., Chen Y.Q., Yu Z., Wang P., Ni D.J. Nonvolatile metabolism in postharvest tea (Camellia sinensis L.) leaves: Effects of different withering treatments on nonvolatile metabolites, gene expression levels, and enzyme activity. Food Chem. 2020;327:126992. doi: 10.1016/j.foodchem.2020.126992. PubMed DOI

Chai F.M., Liu W.W., Xiang Y., Meng X.B., Sun X.M., Cheng C., Liu G.T., Duan L.X., Xin H.P., Li S.H. Comparative metabolic profiling of Vitis amurensis and Vitis vinifera during cold acclimation. Hortic. Res. 2019;6:8. doi: 10.1038/s41438-018-0083-5. PubMed DOI PMC

Zhou P.L., Khan R., Li Q.Y., Liu G.L., Xu N., Yang Y.J., Wang Y., Wang S.S., Chen A.G. Transcriptomic analyses of chilling stress responsiveness in leaves of tobacco (Nicotiana tabacum) seedlings. Plant Mol. Biol. Rep. 2019;38:1–13. doi: 10.1007/s11105-019-01167-0. DOI

Yang Q.S., Wu J.H., Li C.Y., Wei Y.R., Shen O., Hu C.H., Kuang R.B. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB group) seedlings. Mol. Cell. Proteom. 2012;11:1853–1869. doi: 10.1074/mcp.M112.022079. PubMed DOI PMC

Trzcinska-Danielewicz J., Bilska A., Fronk J., Zielenkiewicz P., Jarochowska E., Roszczyk M., Jonczyk M., Axentowicz E., Skoneczny M., Sowinski P. Global analysis of gene expression in maize leaves treated with low temperature. I. Moderate chilling (14 °C) Plant Sci. 2009;177:648–658. doi: 10.1016/j.plantsci.2009.09.001. DOI

Spence A.K., Boddu J., Wang D., James B., Swaminathan K., Moose S.P., Long S.P. Transcriptional responses indicate maintenance of photosynthetic proteins as key to the exceptional chilling tolerance of C4 photosynthesis in Miscanthus × giganteus. J. Exp. Bot. 2014;65:3737–3747. doi: 10.1093/jxb/eru209. PubMed DOI PMC

FAOSTAT. [(accessed on 15 February 2020)];2020 Available online: https://www.fao.org/faostat/en/#data/QC/visualize.

Turner D.W., Lahav E. The growth of banana plants in relation to temperature. Funct. Plant Biol. 1983;10:43–53. doi: 10.1071/PP9830043. DOI

Liu H., Ouyang B., Zhang J.H., Wang T.T., Li H.X., Zhang Y.Y., Yu C.Y., Ye Z.B. Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PLoS ONE. 2012;7:e50785. doi: 10.1371/journal.pone.0050785. PubMed DOI PMC

Xu C.X. Fruit Cultivation in South China. China Agriculture Press; Beijing, China: 2015. pp. 85–86.

Xu C.X., Chen J.Z., Liang L.F. Effects of low temperature on the contents of glycerol, starch and sugars in banana leaves [in Chinese with English abstract] J. Fruit Sci. 2000;17:105–109.

Feng R.J., Zhang L.L., Wang J.Y., Luo J.M., Peng M. Proteomic analysis of cold stress responses in banana leaves. J. Ameri. Soc. Hort. Sci. 2015;140:214–222. doi: 10.21273/JASHS.140.3.214. DOI

Lai Z.X., Chen Y., Lin Y.L., Zhao Q.Y., Chen Y.T. Discovery and taxonomy of wild banana (Musa spp.) in Fuzhou. [in Chinese with an English abstract] Subtrop. Agric. Res. 2007;3:1–5.

Liu W.H., Cheng C.Z., Lin Y.L., Xuhan X., Lai Z.X. Genome-wide identification and characterization of mRNAs and lncRNAs involved in cold stress in the wild banana (Musa itinerans) PLoS ONE. 2018;13:e0200002. doi: 10.1371/journal.pone.0200002. PubMed DOI PMC

Yamori W., Hikosaka K., Way D.A. Temperature response of photosynthesis in C3, C4, and CAM plants: Temperature acclimation and temperature adaptation. Photosynth. Res. 2014;119:101–117. doi: 10.1007/s11120-013-9874-6. PubMed DOI

Sobkowiak A., Jończyk M., Adamczyk J., Szczepanik J., Solecka D., Kuciara I., Hetmańczyk K., Trzcinska-Danielewicz J., Grzybowski M., Skoneczny M., et al. Molecular foundations of chilling-tolerance of modern maize. BMC Genom. 2016;17:125. doi: 10.1186/s12864-016-2453-4. PubMed DOI PMC

Friesen P.C., Sage R.F. Photosynthetic responses to chilling in a chilling-tolerant and chilling-sensitive Miscanthus hybrid. Plant Cell Environ. 2016;39:1420–1431. doi: 10.1111/pce.12699. PubMed DOI

Hajihashemi S., Noedoost F., Geuns J.M.C., Djalovic I., Siddique K.H.M. Effect of cold stress on photosynthetic traits, carbohydrates, morphology, and anatomy in nine cultivars of Stevia rebaudiana. Front. Plant Sci. 2018;9:1430. doi: 10.3389/fpls.2018.01430. PubMed DOI PMC

Nouri M.Z., Moumeni A., Komatsu S. Abiotic stresses: Insight into gene regulation and protein expression in photosynthetic pathways of plants. Int. J. Mol. Sci. 2015;16:20392–20416. doi: 10.3390/ijms160920392. PubMed DOI PMC

Lu J.Y., Nawaz M.A., Wei N.N., Cheng F., Bie Z.L. Suboptimal temperature acclimation enhances chilling tolerance by improving photosynthetic adaptability and osmoregulation ability in watermelon. Hortic. Plant J. 2020;6:49–60. doi: 10.1016/j.hpj.2020.01.001. DOI

Naidu S.L., Moose S.P., AL-Shoaibi A.K., Raines C.A., Long S.P. Cold tolerance of C4 photosynthesis in Miscanthus × giganteus: Adaptation in amounts and sequence of C4 photosynthetic enzymes. Plant Physiol. 2003;132:1688–1697. doi: 10.1104/pp.103.021790. PubMed DOI PMC

Wang D.F., Naidu S.L., Portis A.R., Jr., Moose S.P., Long S.P. Can the cold tolerance of C4 photosynthesis in Miscanthus × giganteus relative to Zea mays be explained by differences in activities and thermal properties of Rubisco? J. Exp. Bot. 2008;59:1779–1787. doi: 10.1093/jxb/ern074. PubMed DOI

Wang D.F., Portis A.R., Moose S.P., Long S.P. Cool C4 photosynthesis: Pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus × giganteus. Plant Physiol. 2008;148:557–567. doi: 10.1104/pp.108.120709. PubMed DOI PMC

Long S.P., Spence A.K. Toward cool C4 crops. Annu. Rev. Plant Biol. 2013;64:701–722. doi: 10.1146/annurev-arplant-050312-120033. PubMed DOI

Bilska-Kos A., Panek P., Szulc-Głaz A., Ochodzki P., Cisło A., Zebrowski J. Chilling-induced physiological, anatomical and biochemical responses in the leaves of Miscanthus × giganteus and maize (Zea mays L.) J. Plant Physiol. 2018;228:178–188. doi: 10.1016/j.jplph.2018.05.012. PubMed DOI

Caffarri S., Frigerio S., Olivieri E., Righetti P.G., Bassi R. Differential accumulation of Lhcb gene products in thylakoid membranes of Zea mays plants grown under contrasting light and temperature conditions. Proteomics. 2005;5:758–768. doi: 10.1002/pmic.200402008. PubMed DOI

Cavaco A.M., De Silva A.B., Arrabaca M.C. Effects of long-term chilling on growth and photosynthesis of the C4 gramineae Paspalum dilatatum. Physiol. Plant. 2003;119:87–96. doi: 10.1034/j.1399-3054.2003.00148.x. DOI

Soares-Cordeiro A.S., Driscoll S.P., Arrabaca M.C., Foyer C.H. Dorsoventral variations in dark chilling effects on photosynthesis and stomatal function in Paspalum dilatatum leaves. J. Exp. Bot. 2010;62:687–699. doi: 10.1093/jxb/erq302. PubMed DOI PMC

Sharma P., Sharma N., Deswal R. The molecular biology of the low-temperature response in plants. Bioessays. 2005;27:1048–1059. doi: 10.1002/bies.20307. PubMed DOI

Yan Y.L., Takác T., Li X.Q., Chen H.B., Wang Y.Y., Xu E.F., Xie L., Su Z.H., Šamaj J., Xu C.X. Variable content and distribution of arabinogalactan proteins in banana (Musa spp.) under low temperature stress. Front. Plant Sci. 2015;6:353. doi: 10.3389/fpls.2015.00353. PubMed DOI PMC

Meng J., Hu B., Yi G.J., Li X.Q., Chen H.B., Wang Y.Y., Yuan W.N., Xing Y.Q., Sheng Q.M., Su Z.X., et al. Genome-wide analyses of banana fasciclin-like AGP genes and their differential expression under low-temperature stress in chilling sensitive and tolerant cultivars. Plant Cell Rep. 2020;39:693–708. doi: 10.1007/s00299-020-02524-0. PubMed DOI

Xia X.J., Wang Y.J., Zhou Y.H., Tao Y., Mao W.H., Shi K., Asami T., Chen Z.X., Yu J.Q. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 2009;150:801–814. doi: 10.1104/pp.109.138230. PubMed DOI PMC

Wang L., Zhang X., Ma Y.H., Qing Y.H., Wang H.C., Huang X.M. The highly drought-tolerant pitaya (Hylocereus undatus) is a non-facultative CAM plant under both well-watered and drought conditions. J. Horticult. Sci. Biotechnol. 2019;94:643–652. doi: 10.1080/14620316.2019.1595747. DOI

Xu C.X., Takáč T., Burbach C., Menzel D., Samaj J. Developmental localization and the role of hydroxyproline rich glycoproteins during somatic embryogenesis of banana (Musa spp. AAA) BMC Plant Biol. 2011;11:38. doi: 10.1186/1471-2229-11-38. PubMed DOI PMC

Niu Y.Q., Hu B., Li X.Q., Chen H.B., Takáč T., Šamaj J., Xu C.X. Comparative digital gene expression analysis of tissue-cultured plantlets of highly resistant and susceptible banana cultivars in response to Fusarium oxysporum. Int. J. Mol. Sci. 2018;19:350. doi: 10.3390/ijms19020350. PubMed DOI PMC

Fang D.L., Yang W.J., Deng Z.L., An X.X., Zhao L.Y., Hu Q.H. Proteomic investigation of metabolic changes of mushroom (Flammulina velutipes) packaged with nanocomposite material during cold storage. J. Agric. Food Chem. 2017;65:10368–10381. doi: 10.1021/acs.jafc.7b04393. PubMed DOI

Oberg A.L., Mahoney D.W., Eckel-Passow J.E., Malone C.J., Wolfinger R.D., Hill E.G., Cooper L.T., Onuma O.K., Spiro C., Therneau T.M., et al. Statistical analysis of relative labeled mass spectrometry data from complex samples using ANOVA. J. Proteome Res. 2008;7:225–233. doi: 10.1021/pr700734f. PubMed DOI PMC

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