Skip to main content
SpringerLink
Log in

Drought stress-induced autophagy gene expression is correlated with carbohydrate concentrations in Caragana korshinskii

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Autophagy has been reported to be an adapt function of plant cells under various stresses. In this report, autophagy-related gene expressions and carbohydrate concentrations in Caragana korshinskii leaf cells under drought stress were investigated. Leaf samples of C. korshinskii plants of an estimated 15-year-old were collected from three sites with different drought stress (annual precipitation range, 325.8 to 440.8 mm) at the Loess Plateau in northwestern China. Autophagy was observed in C. korshinskii samples from all three sites and was revealed by autophagosomes in the cytoplasm of mesophyll cells and increased chloroplasts degradation observed by transmission electron microscopy. Furthermore, with the drought stress increase, autophagy-related gene expressions were upregulated and leaf concentration of sucrose was increased, while concentrations of monosaccharide sugars such as glucose, fructose and galactose were decreased. The results suggested that drought stress induced autophagy gene expression, which may serve as a survival mechanism for nutrient remobilisation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leo’n P. (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14:2085–2096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aubert S, Gout E, Bligny R, Dl M-M, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133:1251–1263

    Article  CAS  PubMed  Google Scholar 

  • Avin-Wittenberg T, Honig A, Galili G (2012) Variations on a theme: plant autophagy in comparison to yeast and mammals. Protoplasma 249:285–299

    Article  CAS  PubMed  Google Scholar 

  • Bai J, Kang T, Wu HD, Lu B, Long X et al (2017) Relative contribution of photorespiration and antioxidative mechanisms in Caragana korshinskii under drought conditions across the Loess Plateau. Funct Plant Biol 44:1111–1123

    Article  CAS  PubMed  Google Scholar 

  • Bassham DC (2007) Plant autophagy: more than a starvation response. Curr Opin Plant Biol 10:587–593

    Article  CAS  PubMed  Google Scholar 

  • Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2014) Autophagy in development and stress responses of plants. Autophagy 2:2–11

    Article  Google Scholar 

  • Bilska-Kos A, Solecka D, Dziewulska A, Ochodzki P, Jonczyk M, Bilski H, Sowinski P (2017) Low temperature caused modifications in the arrangement of cell wall pectins due to changes of osmotic potential of cells of maize leaves (Zea mays L.). Protoplasma 254:713–724

    Article  CAS  PubMed  Google Scholar 

  • Budak H, Kantar M, Kurtoglu KY (2013) Drought tolerance in modern and wild wheat. Sci World J 2013:548246

    Article  Google Scholar 

  • Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to suc starvation. Plant Physiol 135:2330–2347

  • de Sousa DPF, Braga BB, Gondim FA, Gomes-Filho E, Martins K, de Brito POB (2016) Increased drought tolerance in maize plants induced by H2O2 is closely related to an enhanced enzymatic antioxidant system and higher soluble protein and organic solutes contents. Theoretical and Experimental Plant Physiology 28:297–306

  • Fang X, Li J, Xiong Y, Xu D, Fan X, Li F (2007) Responses of Caragana korshinskii Kom. to shoot removal: mechanisms underlying regrowth. Ecol Res 23:863–871

    Article  Google Scholar 

  • Fang XW, Turner NC, Li FM, Li WJ, Guo XS (2011) Caragana korshinskii seedlings maintain positive photosynthesis during short-term, severe drought stress. Photosynthetica 49:603–609

    Article  CAS  Google Scholar 

  • Guehl JM, Clement A, Kaushal P, Aussenac G (1993) Planting stress, water status and non-structural carbohydrate concentrations in Corsican pine seedlings. Tree Physiol 12:173–183

    Article  CAS  PubMed  Google Scholar 

  • Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282:37298–37302

    Article  CAS  PubMed  Google Scholar 

  • Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129:1181–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayward AP, Tsao J, Dinesh-Kumar SP (2009) Autophagy and plant innate immunity: defense through degradation. Semin Cell Dev Biol 20:1041–1047

    Article  CAS  PubMed  Google Scholar 

  • Ishida H, Izumi M, Wada S, Makino A (2014) Roles of autophagy in chloroplast recycling. Biochim Biophys Acta 1837:512–521

    Article  CAS  PubMed  Google Scholar 

  • Ishida H, Yoshimoto K (2014) Chloroplasts are partially mobilized to the vacuole by autophagy. Autophagy 4:961–962

    Article  Google Scholar 

  • Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008) Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koppenaa RS, Tschaplin TJ, Colomb SJ (1991) Carbohydrate accumulation and turgor maintenance in seedling shoots and roots of two boreal conifers subjected to water stress. Can J Bot 69:2522–2528

    Article  Google Scholar 

  • Kroemer K, Mariño G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40:280–293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9:e1003790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xiong Y, Bassham DC (2014) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963

    Article  Google Scholar 

  • Luo XJ, Liu XH, Wang CY, Wang XY (2008) Formation of membrane-bound inclusions and their associations with cytoplasmic channels in early prophase male meiocytes of Althaea rosea (L.) Cavan Cell Biol Int 32:374–383

  • McCarthy A, Chung M, Ivanov AG, Krol M, Inman M, Maxwell DP, Hüner NPA (2016) An established Arabidopsis thaliana var. Landsberg erecta cell suspension culture accumulates chlorophyll and exhibits a stay-green phenotype in response to high external sucrose concentrations. J Plant Physiol 199:40–51

    Article  CAS  PubMed  Google Scholar 

  • Mehrpour M, Esclatine A, Beau I, Codogno P (2010) Overview of macroautophagy regulation in mammalian cells. Cell Res 20:748–762

    Article  PubMed  Google Scholar 

  • Mizushima N (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22:132–139

    Article  CAS  PubMed  Google Scholar 

  • Mohammadkhani N, Heidari R (2008) Drought-induced accumulation of soluble sugars and proline in two maize varieties. World Appl Sci J 3:448–453

    Google Scholar 

  • Pu Y, Bassham DC (2013) Links between ER stress and autophagy in plants. Plant Signal Behav 8:e24297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qadir M, Bibi A, Tahir MH, Saleem M, Sadaqat HA (2015) Screening of sorghum (Sorghum bicolor L) genotypes under various levels of drought stress. Maydica 60

  • Sanders GJ, Arndt SK (2012) Osmotic adjustment under drought conditions. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, Heidelberg, pp 199–229

    Chapter  Google Scholar 

  • Secchi F, Zwieniecki MA (2016) Accumulation of sugars in the xylem apoplast observed under water stress conditions is controlled by xylem pH. Plant Cell Environ 39:2350–2360

  • Slavikova S, Shy G, Yao Y, Glozman R, Levanony H, Pietrokovski S, Elazar Z, Galili G (2005) The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J Exp Bot 56:2839–2849

    Article  CAS  PubMed  Google Scholar 

  • Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 20:5971–5981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki K, Kubota Y, Sekito T, Ohsumi Y (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12:209–218

    Article  CAS  PubMed  Google Scholar 

  • Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 119:301–311

  • Tanida I (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 14:2201

    Article  CAS  PubMed  Google Scholar 

  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138:2097–2110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tkn W, Blake TJ, Boyle TJB (1992) Drought tolerance in faster- and slower-growing black spruce (Picea mariana) progenies: II. Osmotic adjustment and changes of soluble carbohydrates and amino acids under osmotic stress. Physiol Plant 85:645–651

    Article  Google Scholar 

  • Tognetti JA, Pontis HG, Martínez-Noël GA (2013) Sucrose signaling in plants, a world yet to be explored. Plant Signal Behav 8:e23316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Doorn WG (2008) Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels. J Exp Bot 59:1963–1972

    Article  PubMed  CAS  Google Scholar 

  • Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2008) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149:885–893

    Article  PubMed  Google Scholar 

  • Wang P, Sun X, Wang N, Tan D-X, Ma F (2015) Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J Pineal Res 58:479–489

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Blumwald E (2014) Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell 26:4875–4888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, Huang L, Du Y, Hong Y, Tang D, Liu Y (2013) Autophagy contributes to leaf starch degradation. Plant Cell 25:1383–1399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20:264–265

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42:535–546

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143:291–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan H, Hu X, Li F (2012) Leaf photosynthesis, chlorophyll fluorescence, ion content and free amino acids in Caragana korshinskii Kom exposed to NaCl stress. Acta Physiol Plant 34:2285–2295

    Article  CAS  Google Scholar 

  • Yang Q, Yin J, Li G, Qi L, Yang F, Wang R (2014) Reference gene selection for qRT-PCR in Caragana korshinskii Kom. under different stress conditions. Mol BiolRep 41:2325–2334

    CAS  Google Scholar 

  • Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1–32

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Klionsky DJ (2010) Eaten alive: a history of macroautophagy. Nat Cell Biol 12:814–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimoto K, Takano Y, Sakai Y (2010) Autophagy in plants and phytopathogens. FEBS Lett 584:1350–1358

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu M, Monroe JG, Suhail Y, Villiers F, Mullen J, Pater D (2016) Molecular and systems approaches towards drought-tolerant canola crops. New Phytol 210:1169–1189

Download references

Funding

The work was funded by the National Natural Science Foundation of China (31100455 and 31301797) and the Natural Science Basic Research Plan in Shaanxi Province of China (2016JQ3006).

Author information

Authors and Affiliations

  1. College of Life Sciences, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Xinjuan Luo & Hongdou Wu

  2. College of Sciences, Northwest A&F University, 712100, Yangling, Shaanxi, China

    Yanyu Zhang

  3. College of Horticulture, Northwest A&F University, 712100, Yangling, Shaanxi, China

    Juan Bai

Authors
  1. Xinjuan Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanyu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongdou Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Bai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Néstor Carrillo

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, X., Zhang, Y., Wu, H. et al. Drought stress-induced autophagy gene expression is correlated with carbohydrate concentrations in Caragana korshinskii. Protoplasma 257, 1211–1220 (2020). https://doi.org/10.1007/s00709-020-01507-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01507-y

Keywords

Search

Navigation