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Characterization and differential expression of sucrose and starch metabolism genes in contrasting chickpea (Cicer arietinum L.) genotypes under low temperature

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Abstract

Low temperature (LT) causes significant yield losses in chickpea (Cicer arietinum L.). The sucrose starch metabolism is associated with abiotic-stress tolerance or sensitivity in plants. The changes in sugars and starch contents under LT in chickpea have already been studied, however, no information is available on LT-induced alterations in transcription of carbohydrate metabolic pathway genes in chickpea. To understand the differences in the regulation of sucrose and starch metabolism under LT, the expression of sucrose and starch metabolism genes was studied in leaves of cold-sensitive (GPF2) and cold-tolerant (ICC 16349) chickpea genotypes. The mRNA sequences of chickpea genes were retrieved from the public databases followed by confirmation of identity and characterization. All the genes were functional in chickpea. Between the two paralogues of cell wall invertase, cell wall invertase 3×2 (CWINx2) was the truncated version of cell wall invertase 3×1 (CWINx1) with the loss of 241 bases in the mRNA and 67 amino acids at N terminal of the protein. Comparison of expression of the genes between control (22°C day / 16°C night) and LT treated (4°C; 72 h) plants revealed that granule bound starch synthase 2 (GBSS2) and β-amylase 3 (BAM3) were upregulated in ICC 16349 whereas sucrose phosphate synthase 2 (SPS2), CWINx1, CWINx2 and β-amylase 1 (BAM1) were downregulated. In contrast to this, SPS2, CWINx1, CWINx2 and BAM1 were upregulated and GBSS2 downregulated in GPF2 under LT. The gene expression data suggested that UGPase, CWINs, GBSS2 and BAM3 are important components of cold-tolerance machinery of chickpea.

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References

  • Asaoka M., Okuno K. and Fuwa H. 1985 Effect of environmental temperature at the milky stage on amylose content and fine structure of amylopectin of waxy and nonwaxy endosperm starches of rice (Oryza sativa L.). Agric. Biol. Chem. 49, 373–379.

    CAS  Google Scholar 

  • Bhandari K., Sharma K. D., Rao B. H., Siddique K. H., Gaur P., Agrawal S. K. et al. 2017 Temperature sensitivity of food legumes: a physiological insight. Acta Physiol. Plant. 39, 68.

    Article  CAS  Google Scholar 

  • Borovkov A. Y., Mcclean P. E., Sowokinos J. R., Ruud S. H. and Secor G. A. 1996 Effect of expression of UDP-glucose pyrophosphorylase ribozyme and antisense RNAs on the enzyme activity and carbohydrate composition of field-grown transgenic potato plants. J. Plant Physiol. 147, 644–652.

    Article  CAS  Google Scholar 

  • Catalán A., Glaser-Schmitt A., Argyridou E., Duchen P. and Parsch J. 2016 An indel polymorphism in the MtnA 3′untranslated region is associated with gene expression variation and local adaptation in Drosophila melanogaster. PLoS Genet. 12, e1005987.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng W. H., Earl W. T. and Prem S. C. 1999 Sugars modulate an unusual mode of control of the cell-wall invertase gene (Incw1) through its 3′ untranslated region in a cell suspension culture of maize. Proc. Natl. Acad. Sci. USA 96, 10512–10517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V., Zhu J. and Zhu J. K. 2007 Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444–451.

    Article  CAS  PubMed  Google Scholar 

  • Ciereszko I., Johansson H. and Kleczkowski L. A. 2001 Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem. J. 354, 67–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dèjardin A., Sokolov L. N. and Kleczkowski L. A. 1999 Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem. J. 344, 503–509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deryabin A. N., Dubinina I. M., Burakhanova E. A., Astakhova N. V., Sabel’nikova E. P. and Trunova T. I. 2005 Influence of yeast-derived invertase gene expression in potato plants on membrane lipid peroxidation at low temperature. J. Therm. Biol. 30, 73–77.

    Article  CAS  Google Scholar 

  • Dinari A., Niazi A., Afsharifar A. R. and Ramezani A. 2013 Identification of upregulated genes under cold stress in cold-tolerant chickpea using the cDNA-AFLP approach. PLoS One 8, 1–7.

    Article  CAS  Google Scholar 

  • Dong S. and Beckles D. M. 2019 Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J. Plant Physiol. 234, 80–93.

    Article  PubMed  CAS  Google Scholar 

  • Edner C., Li J., Albrecht T., Mahlow S., Hejazi M., Hussain H., Kaplan F. et al. 2007 Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol. 145, 17–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Essmann J., Schmitz-Thom I., Schön H., Sonnewald S., Weis E. and Scharte J. 2008 RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol. 147, 1288–1299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Führing J., Cramer J. T., Routier F. H., Lamerz A. C., Baruch P., Gerardy-Schahn R. and Fedorov R. 2013 Catalytic mechanism and allosteric regulation of UDP-glucose pyrophosphorylase from Leishmania major. ACS Catal. 3, 2976–2985.

    Article  CAS  Google Scholar 

  • Garg R., Bhattacharjee A. and Jain M. 2015 Genome-scale transcriptomic insights into molecular aspects of abiotic stress responses in chickpea. Plant Mol. Biol. Rep. 33, 388–400.

    Article  CAS  Google Scholar 

  • Gaur P. M., Krishnamurthy L. and Kashiwagi J. 2008 Improving drought-avoidance root traits in chickpea (Cicer arietinum L.)-current status of research at ICRISAT. Plant Prod. Sci. 11, 3–11.

    Article  Google Scholar 

  • Gupta S. K. and Sowokinos J. R. 2003 Physicochemical and kinetic properties of unique isozymes of UDP-Glc pyrophosphorylase that are associated with resistance to sweetening in cold-stored potato tubers. J. Plant Physiol. 160, 589–600.

    Article  CAS  PubMed  Google Scholar 

  • Guy C. L., Huber J. L. and Huber S. C. 1992 Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol. 100, 502–508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill L. M., Reimholz R., Schröder R., Nielsen T. H. and Stitt M. 1996 The onset of sucrose accumulation in cold-stored potato tubers is caused by an increased rate of sucrose synthesis and coincides with low levels of hexose-phosphates, an activation of sucrose phosphate synthase and the appearance of a new form of amylase. Plant Cell Environ. 19, 1223–1237.

    Article  CAS  Google Scholar 

  • Hirano H. Y. and Sano Y. 1998 Enhancement of Wx gene expression and the accumulation of amylose in response to cool temperatures during seed development in rice. Plant Cell Physiol. 39, 807–812.

    Article  CAS  Google Scholar 

  • Jain M., Misra G., Patel R. K., Priya P., Jhanwar S., Khan A. W. et al. 2013 A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 74, 715–729.

    Article  CAS  PubMed  Google Scholar 

  • Jha U. C., Chaturvedi S. K., Bohra A., Basu P. S., Khan M. S. and Barh D. 2014 Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breed. 133, 163–178.

    Article  Google Scholar 

  • Jung S. H., Lee J. Y. and Lee D. H. 2003 Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Mol. Biol. 52, 553–567.

    Article  CAS  PubMed  Google Scholar 

  • Kohli D., Joshi G., Deokar A. A., Bhardwaj A. R., Agarwal M., Katiyar-Agarwal S. et al. 2014 Identification and characterization of wilt and salt stress-responsive microRNAs in chickpea through high-throughput sequencing. PLoS One 9, e108851.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koide T., Ohnishi Y. and Horinouchi S. 2011 Characterization of recombinant beta-amylases from Oryza sativa. Biosci. Biotechnol. Biochem. 75, 793–796.

    Article  CAS  PubMed  Google Scholar 

  • Kaloki P., Devasirvatham V. and Tan D. K. 2019 Chickpea Abiotic Stresses: combating drought, heat and cold. In Abiotic and biotic stress in plants. IntechOpen (https://doi.org/10.5772/intechopen.83404).

  • Kaplan F. and Guy C. L. 2004 β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 135, 1674–1684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan F., Sung D. Y. and Guy C. L. 2006 Roles of β-amylase and starch breakdown during temperatures stress. Physiol. Plant. 126, 120–128.

    Article  CAS  Google Scholar 

  • Kaur G., Kumar S., Nayyar H. and Upadhyaya H. D. 2008 Cold stress injury during the pod-filling phase in chickpea (Cicer arietinum L.): Effects on quantitative and qualitative components of seeds. J. Agron. Crop Sci. 194, 457–464.

    Google Scholar 

  • Kaur S., Gupta A. K., Kaur N., Sandhu J. S. and Gupta S. K. 2009 Antioxidative enzymes and sucrose synthase contribute to cold stress tolerance in chickpea. J. Agron. Crop Sci. 195, 393–397.

    Article  CAS  Google Scholar 

  • Kazemi-Shahandashti S. S., Maali-Amiri R., Zeinali H., Khazaei M., Talei A. and Ramezanpour S. S. 2014 Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings. J. Plant Physiol. 171, 1106–1116.

    Article  CAS  PubMed  Google Scholar 

  • Kiran A., Kumar S., Nayyar H. and Sharma K. D. 2019 Low temperature-induced aberrations in male and female reproductive organ development cause flower abortion in chickpea. Plant Cell Environ. 42, 2075–2089.

    Article  CAS  PubMed  Google Scholar 

  • Kiran A., Sharma P. N., Awasthi R., Nayyar H., Seth R., Chandel S. S., Siddique K. H., Zinta G. and Sharma K. D. 2021 Disruption of carbohydrate and proline metabolism in anthers under low temperature causes pollen sterility in chickpea. Environ. Exp. Bot., https://doi.org/10.1016/j.envexpbot.2021.104500.

    Article  Google Scholar 

  • Kleczkowski L. A., Geisler M., Ciereszko I. and Johansson H. 2004 UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol. 134, 912–918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klotke J., Kopka J., Gatzke N. and Heyer A. G. 2004 Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation–evidence for a role of raffinose in cold acclimation. Plant Cell Environ. 27, 1395–1404.

    Article  CAS  Google Scholar 

  • Kossmann J. and Lloyd J. 2000 Understanding and influencing starch biochemistry. Crit. Rev. Plant Sci. 19, 171–226.

    Article  CAS  Google Scholar 

  • Kumar S., Nayyar H., Bhanwara R. K. and Upadhyaya H. D. 2010 Chilling stress effects on reproductive biology of chickpea. J. SAT Agric. Res. 8, 1–14.

    CAS  Google Scholar 

  • Kumar S., Malik J., Thakur P., Kaistha S., Sharma K. D., Upadhyaya H. D. et al. 2011 Growth and metabolic responses of contrasting chickpea (Cicer arietinum L.) genotypes to chilling stress at reproductive phase. Acta Physiol. Plant. 33, 779–787.

    Article  CAS  Google Scholar 

  • Kumar S., Thakur P., Kaushal N., Malik J. A., Gaur P. and Nayyar H. 2013 Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity. Arch. Agron. Soil Sci. 59, 823–843.

    Article  CAS  Google Scholar 

  • Liu M., Shi J. and Lu C. 2013 Identification of stress-responsive genes in Ammopiptanthus mongolicus using ESTs generated from cold-and drought-stressed seedlings. BMC Plant Biol. 13, 88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levitt J. 1980 Responses of Plants to Environmental Stresses. In Water, radiation, salt and other stress, pp. 93–128. Field Crops Research, Academic Press, New York.

  • Mantri N. L., Ford R., Coram T. E. and Pang E. C. 2010 Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environ. Exp. Bot. 69, 286–292.

    Article  Google Scholar 

  • Meng M., Geisler M., Johansson H., Mellerowicz E. J., Karpinski S. and Kleczkowski L. A. 2007 Differential tissue/organ-dependent expression of two sucrose-and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus. Gene. 389, 186–195.

    Article  CAS  PubMed  Google Scholar 

  • Mo Y., Liang G., Shi W. and Xie J. 2011 Metabolic responses of alfalfa (Medicago sativa L.) leaves to low and high temperature induced stresses. Afr. J. Biotechnol. 10, 1117–1124.

    CAS  Google Scholar 

  • Muehlbauer F. J. and Rajesh P. N. 2008 Chickpea, a common source of protein and starch in the semi-arid ropics. In Genomics of tropical crop plants, pp. 171-186. Springer, New York.

  • Nägele T. and Heyer A. G. 2013 Approximating subcellular organisation of carbohydrate metabolism during cold acclimation in different natural accessions of Arabidopsis thaliana. New Phytol. 198, 777–787.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen T. H., Deiting U. and Stitt M. 1997 A [beta]-amylase in potato tubers is induced by storage at low temperature. Plant Physiol. 113, 503–510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver S. N., Van Dongen J. T., Alfred S. C., Mamun E. A., Zhao X., Saini H. S. et al. 2005 Cold-induced repression of the rice anther specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ. 28, 1534–1551.

    Article  CAS  Google Scholar 

  • Oufir M., Legay S., Nicot N., Van Moer K., Hoffmann L., Renaut J. et al. 2008 Gene expression in potato during cold exposure: changes in carbohydrate and polyamine metabolisms. Plant Sci. 175, 839–852.

    Article  CAS  Google Scholar 

  • Parish R. W., Phan H. A., Iacuone S. and Li S. F. 2012 Tapetal development and abiotic stress: a centre of vulnerability. Funct. Plant Biol. 39, 553–559.

    Article  CAS  PubMed  Google Scholar 

  • Park S. H., Jeong J. S., Redillas M. C., Jung H., Bang S. W., Kim Y. S. and Kim J. K. 2013 Transgenic overexpression of UIP1, an interactor of the 3′ untranslated region of the Rubisco small subunit mRNA, increases rice tolerance to drought. Plant Biotechnol. Rep. 7, 83–90.

    Article  Google Scholar 

  • Rani A., Devi P., Jha U. C., Sharma K. D., Siddique K. H. M. and Nayyar H. 2019 Developing climate-resilient chickpea involving physiological and molecular approaches with a focus on temperature and drought stresses. Front. Plant Sci. 10, 1759.

    Article  PubMed  Google Scholar 

  • Reimholz R., Geiger M., Haake V., Deiting U., Krause K. P., Sonnewald U. and Stitt M. 1997 Potato plants contain multiple forms of sucrose phosphate synthase, which differ in their tissue distributions, their levels during development, and their responses to low temperature. Plant Cell Environ. 20, 291–305.

    Article  CAS  Google Scholar 

  • Rosa M., Prado C., Podazza G., Interdonato R., González J. A., Hilal M. and Prado F. E. 2009 Soluble sugars: Metabolism, sensing and abiotic stress: A complex network in the life of plants. Plant Signal. Behav. 4, 388–393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruelland E., Cantrel C., Gawer M., Kader J. C. and Zachowski A. 2002 Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol. 130, 999–1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki H., Ichimura K., Imada S. and Yamaki S. 2001 Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings. J. Plant Physiol. 158, 847–852.

    Article  CAS  Google Scholar 

  • Savitch L. V., Gray G. R. and Huner N. P. 1997 Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201, 18–26.

    Article  CAS  Google Scholar 

  • Savitch L. V., Harney T. and Huner N. P. 2000 Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation. Physiol. Plant. 108, 270–278.

    Article  CAS  Google Scholar 

  • Seki M., Narusaka M., Abe H., Kasuga M., Yamaguchi-Shinozaki K., Carninci P. et al. 2001 Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13, 61–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma K. K. and Lavanya M. 2002 Recent developments in transgenics for abiotic stress in legumes of the semi-arid tropics. JIRCAS Working Report No. 23. 23, 61–73.

  • Sharma K. D. and Nayyar H. 2014 Cold stress alters transcription in meiotic anthers of cold tolerant chickpea (Cicer arietinum L.). BMC Res. Notes. 7, 717.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma K. D. and Nayyar H. 2016 Regulatory networks in pollen development under cold stress. Front. Plant Sci. 7, 402.

    Article  PubMed  PubMed Central  Google Scholar 

  • Slugina M. A., Shchennikova A. V. and Kochieva E. Z. 2017 TAI vacuolar invertase orthologs: the interspecific variability in tomato plants (Solanum section Lycopersicon). Mol. Genet. Genom. 292, 1123–1138.

    Article  CAS  Google Scholar 

  • Slugina M. A., Shchennikova A. V. and Kochieva E. Z. 2018 LIN7 cell-wall invertase orthologs in cultivated and wild tomatoes (Solanum section Lycopersicon). Plant Mol. Biol. Rep. 36, 195–209.

    Article  CAS  Google Scholar 

  • Sofi S. A., Singh J., Chhikara N. and Panghal A. 2020 Effect of incorporation of germinated flour and protein isolate from chickpea on different quality characteristics of rice-based noodle. Cereal Chem. 97, 85–94.

    Article  CAS  Google Scholar 

  • Sowokinos J. R., Thomas C. and Burrell M. M. 1997 Pyrophosphorylases in Potato (V. Allelic Polymorphism of UDP-Glucose Pyrophosphorylase in Potato Cultivars and Its Association with Tuber Resistance to Sweetening in the Cold). Plant Physiol. 113, 511–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spychalla J. P., Scheffler B. E., Sowokinos J. R. and Bevan M. W. 1994 Cloning, antisense RNA inhibition, and the coordinated expression of UDP-glucose pyrophosphorylase with starch biosynthetic genes in potato tubers. J. Plant Physiol. 144, 444–453.

    Article  CAS  Google Scholar 

  • Strand Å., Hurry V., Gustafsson P. and Gardeström P. 1997 Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J. 3, 605–614.

    Article  Google Scholar 

  • Strand Å., Foyer C. H., Gustafsson P., Gardeström P. and Hurry V. 2003 Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ. 26, 523–535.

    Article  CAS  Google Scholar 

  • Sung D. Y. 2001 Characterization of Arabidopsis heat shock protein 70 (Hsp70) gene family and microarray analysis of gene expression in response to temperature extremes. Ph.D. dissertation, University of Florida, Florida.

  • Suzuki Y., Sano Y. and Hirano H. Y. 2002 Isolation and characterization of a rice mutant insensitive to cool temperatures on amylose synthesis. Euphytica 123, 95–100.

    Article  CAS  Google Scholar 

  • Tang G. Q., Luscher M. and Sturm A. 1999 Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11, 177–189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur A., Sharma K. D., Siddique K. H. and Nayyar H. 2020 Cold priming the chickpea seeds imparts reproductive cold tolerance by reprogramming the turnover of carbohydrates, osmo-protectants and redox components in leaves. Sci. Horti. 261, 108929.

    Article  CAS  Google Scholar 

  • Tesfaye K., Walker S. and Tsubo M. 2006 Radiation interception and radiation use efficiency of three grain legumes under water deficit conditions in a semi-arid environment. Eur. J. Agron. 25, 60–70.

    Article  Google Scholar 

  • Usadel B., Bläsing O. E., Gibon Y., Retzlaff K., Höhne M., Günther M. and Stitt M. 2008 Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol. 146, 1834–1861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varol I. S., Kardes Y. M., Irik H. A., Kirnak H. and Kaplan M. 2020 Supplementary irrigations at different physiological growth stages of chickpea (Cicer arietinum L.) change grain nutritional composition. Food Chem. 303, 125402.

    Article  CAS  PubMed  Google Scholar 

  • Varshney R. K., Song C., Saxena R. K., Azam S., Yu S., Sharpe A. G. et al. 2013 Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat. Biotechnol. 31, 24–26.

    Article  CAS  Google Scholar 

  • Wang S. J., Liu L. F., Chen C. K. and Chen L. W. 2006 Regulations of granule-bound starch synthase I gene expression in rice leaves by temperature and drought stress. Biol. Plant. 50, 537–541.

    Article  CAS  Google Scholar 

  • Wang K., Shao X., Gong Y., Zhu Y., Wang H., Zhang X. et al. 2013 The metabolism of soluble carbohydrates related to chilling injury in peach fruit exposed to cold stress. Postharvest Boil. Technol. 86, 53–61.

    Article  CAS  Google Scholar 

  • Winter H. and Huber S. C. 2000 Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit. Rev. Plant Sci. 19, 31–67.

    Article  CAS  Google Scholar 

  • Xu X. X., Hu Q., Yang W. N. and Jin Y. 2017 The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato. BMC Plant Biol. 17, 1–3.

    Article  CAS  Google Scholar 

  • Xu F., Wang K., Yuan W., Xu W., Liu S., Kronzucker H. J. et al. 2019 Overexpression of rice aquaporin OsPIP1; 2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport. J. Exp. Bot. 70, 671–681.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K. and Shinozaki K. 2006 Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781–803.

    Article  CAS  PubMed  Google Scholar 

  • Yue C., Cao H. L., Wang L., Zhou Y. H., Huang Y. T., Hao X. Y. et al. 2015 Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol. Biol. 88, 591–608.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge financial support received from the Department of Biotechnology, GOI, New Delhi (grant number: BT/PR12371/AGR/2/901/2015).

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SHARMA, K.D., PATIL, G. & KIRAN, A. Characterization and differential expression of sucrose and starch metabolism genes in contrasting chickpea (Cicer arietinum L.) genotypes under low temperature. J Genet 100, 71 (2021). https://doi.org/10.1007/s12041-021-01317-y

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