The Sucrose Starvation Signal Mediates Induction of Autophagy- and Amino Acid Catabolism-Related Genes in Cowpea Seedling


In higher plants, autophagy is bulk degradation process in vacuole necessary for survival under nutrient-limited conditions and plays important roles in senescence, development and pathogenic response, etc. Cowpea is one of the most important legume crops in semi-aride region, which is highly tolerant to drought stress. Changes of photoassimilate status by drought stress and/or sink-source balance appeared to affect autophagy and senescence of leaf in cowpea. Accordingly, we focused on roles of sucrose signal in autophagy and amino acid recycling in cowpea. Effects of starvation stress on the expression of autophagy-related genes (ATGs) and amino acid catabolism-related genes in cowpea [Vigna unguiculata (L.) Walp] were examined by Reverse transcription-polymerase chain reaction (RT-PCR) and anti-ATG8i specific antibody. Sucrose starvation stress enhanced the expression levels of VuATG8i, VuATG8c and VuATG4 incowpea seedlings. The expressions of amino acid catabolism related genes, such as asparagine synthase (VuASN1), proline dehydrogenase1 (VuProDH) and branched chain amino acid transaminase (VuBCAT2), are also up-regulated under the sucrose starvation. In contrast, high sucrose condition suppressed autophagy and the expressions of ATGs. These results indicate that sucrose starvation stress stimulates both autophagy and amino acid catabolism by regulation of ATGs and VuBCAT2. It is conceivable that sucrose starvation stress enhances autophagy in cowpea, possibly via branched chain amino acid level regulated by the starvation-induced BCAT.

Share and Cite:

A. Kaneko, E. Noguchi, Y. Ishibashi, T. Yuasa and M. Iwaya-Inoue, "The Sucrose Starvation Signal Mediates Induction of Autophagy- and Amino Acid Catabolism-Related Genes in Cowpea Seedling," American Journal of Plant Sciences, Vol. 4 No. 3, 2013, pp. 647-653. doi: 10.4236/ajps.2013.43083.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] A. Ciechanover, “The Ubiquitin-Proteasome Pathway: On Protein Death and Cell Life,” The EMBO Journal, Vol. 17, No. 24, 1998, pp. 7151-7160. doi:10.1093/emboj/17.24.7151
[2] Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi and T. Yoshimori, “LC3, a Mammalian Homologue of Yeast Apg8p, Is Localized in Autophagosome Membranes after Processing,” The EMBO Journal, Vol. 19, No. 21, 2000, pp. 5720-5728. doi:10.1093/emboj/19.21.5720
[3] D. J. Klionsky, J. M. Cregg, W. A. Dunn Jr., S. D. Emr, Y. Sakai, I. V. Sandoval, A. Sibirny, S. Subramani, M. Thumm, M. Veenhuis and Y. Ohsumi, “A Unified Nomenclature for Yeast Autophagy-Related Genes,” Developmental Cell, Vol. 5, No. 4, 2003, pp. 539-545. doi:10.1016/S1534-5807(03)00296-X
[4] Y. Ohsumi, “Molecular Dissection of Autophagy: Two Ubiquitin-Like Systems,” Nature Reviews in Molecular Cell Biology, Vol. 2, No. 3, 2001, pp. 211-216. doi:10.1038/35056522
[5] T. Kirisako, Y. Ichimura, H. Okada, Y. Kabeya, N. Mizushima, T. Yoshimori, M. Ohsumi, T. Takao, T. Noda and Y. Ohsumi, “The Reversible Modification Regulates the Membrane-Binding State of Apg8/Aut7 Essential for Autophagy and the Cytoplasm to Vacuole Targeting Path-way,” Journal of Cell Biology, Vol. 151, No. 2, 2000, pp. 263-276. doi:10.1083/jcb.151.2.263
[6] Y. Chen and D. J. Klionsky, “The Regulation of Autophagy—Unanswered Questions,” Journal of Cell Science, Vol. 124, No. 2, 2011, pp. 161-170. doi:10.1242/jcs.064576
[7] C. Robaglia, M. Thomas and C. Meyer, “Sensing Nutrient and Energy Status by SnRK1 and TOR Kinases,” Current Opinion in Plant Biology, Vol. 15, No. 3, 2012, pp. 301-307. doi:10.1016/j.pbi.2012.01.012
[8] S. Slavikova, G. Shy, Y. Yao, R. Glozman, H. Levanony, S. Pietrokovski, Z. Elazar and G. Galili, “The Autophagy-Associated Atg8 Gene Family Operates Both Under Favorable Growth Conditions and under Starvation Stresses in Arabidopsis Plants,” Journal of Experimental Botany, Vol. 56, No. 421, 2005, pp. 2839-2849. doi:10.1093/jxb/eri276
[9] T. L. Rose, L. Bonneau, C. Der, D. Marty-Mazars and F. Marty, “Starvation-Induced Expression of Autophagy-Related Genes in Arabidopsis,” Biology of the Cell, Vol. 98, No. 1, 2006, pp. 53-67. doi:10.1042/BC20040516
[10] H. Rouached, A. B. Arpat and Y. Poirier, “Regulation of Phosphate Starvation Responses in Plants: Signaling Players and Cross-Talks,” Molecular Plant, Vol. 3, No. 2, pp. 288-299. doi:10.1093/mp/ssp120
[11] M. P. S. H. Nang, T. Yuasa, Y. Ishibashi, M. Okuda, H. Tanigawa, S. H. Zheng and M. Iwaya-Inoue, “Leaf Senescence of Soybean at Reproductive Stage Is Associated with Induction of Autophagy-Related Genes, GmATG8c, GmATG8i and GmATG4,” Plant Production Science, Vol. 14, No. 2, 2011, pp. 141-147. doi:10.1626/pps.14.141
[12] J. D. Ehlers and A. E. Hall, “Cowpea (Vigna unguiculata L. Walp.),” Field Crops Research, Vol. 53, No. 1, 1997, pp. 187-204. doi:10.1016/S0378-4290(97)00031-2
[13] M. Arimura, Y. Hashiguchi, M. Imamura, T. Yamaguchi, T. Yuasa and M. Iwaya-Inoue, “Effect of Drought Stress on Carbohydrate Status in Leaves and Seeds of Cowpea during Pod Filling Stage,” Japanese Journal of Crop Science, Vol. 226, No. 2, 2008, pp. 260-261.
[14] T. Sakamoto, Y. Hashigchi, E. Kurauchi, M. Imamura, Y. Ishibashi, S. Muranaka, T. Yuasa and M. Iwaya-Inoue, “Causative Factors of Decreasing Flower Number in Cowpea under Drought Stress during Flowering Stage,” Crybiology and Cryotechnology, Vol. 58, No. 1, 2012, pp. 81-85.
[15] M. P. S. H. Nang, H. Tanigawa, Y. Ishibashi, S. H. Zheng, T. Yuasa and M. Iwaya-Inoue, “Nutrient Starvation Differentially Regulates the Autophagy-Related Gene GmATG8i in Soybean Seedlings,” Plant Biotechnology, Vol. 26, No. 3, 2009, pp. 317-326. doi:10.5511/plantbiotechnology.26.317
[16] J. Nakamura, T. Yuasa, H. T. Tran, K. Harano, S. Tanaka, T. Iwata, T. T. Phan and M. Iwaya-Inoue, “Rice Homologs of Inducer of CBF Expression (OsICE) Are Involved in Cold Acclimation,” Plant Biotechnology, Vol. 28, No. 3, 2011, pp. 303-309. doi:10.5511/plantbiotechnology.11.0421a
[17] M. Okuda, M. P. Nang, K. Oshima, Y. Ishibashi, S. H. Zheng, T. Yuasa and M. Iwaya-Inoue, “The Ethylene Signal Mediates Induction of GmATG8i in Soybean Plants under Starvation Stress,” Bios-cience Biotechnology Biochemistry, Vol. 75, No. 7, 2011, pp. 1408-1412. doi:10.1271/bbb.110086
[18] K. Nakashima, R. Satoh, T. Kiyosue, K. Yamaguchi-Shinozaki and K. Shinozaki, “A Gene Encoding Proline Dehydrogenase Is Not Only Induced by Pro-line and Hypoosmolarity, but Is Also Developmentally Regu-lated in the Reproductive Organs of Arabidopsis,” Plant Physiology, Vol. 118, No. 4, 1998, pp. 1233-1241. doi:10.1104/pp.118.4.1233
[19] M. Malatrasi, M. Corradi, J. T. Svensson, J. Close, M. Gull and N. Marmiroli, “A Branched-Chain Amino Acid Aminotransferase Gene Isolated from Hordeum Vulgare Is Differentially Regulated by Drought Stress,” Theoretical Applied Genetics, Vol. 113, No. 6, 2006, pp. 965-976. doi:10.1007/s00122-006-0339-6
[20] K. Dietrich, F. Weltmeier, A. Ehlert, C. Weiste, M. Stahl, K. Harter and W. Droge-Laser, “Heterodimers of the Arabidopsis Transcription Factors bZIP1 and bZIP53 Reprogram Amino Acid Metabolism during Low Energy Stress,” Plant Cell, Vol. 23, No. 1, 2011, pp. 381-395. doi:10.1105/tpc.110.075390?
[21] A. Guiboileau, K. Yoshimoto, F. Soulay, M. P. Bataille, J. C. Avice and C. Masclaux-Daubresse, “Autophagy Machinery Controls Nitrogen Remobilization at the Whole-Plant Level under Both Limiting and Ample Nitrate Conditions in Arabidopsis,” New Phytologist, Vol. 194, No. 3, 2012, pp. 732-740. doi:10.1111/j.1469-8137.2012.04084.x
[22] J. H. Doelling, J. M. Walker, E. M. Friedman, A. R. Thompson and R. D. Vierstra, “The APG8/12-Activating Enzyme APG7 Is Required for Proper Nutrient Recycling and Senescence in Arabidopsis thaliana,” Journal of Biological Chemistry, Vol. 277, No. 36, 2002, pp. 33105-33114. doi:10.1074/jbc.M204630200
[23] K. Yo-shimoto, H. Hanaoka, S. Sato, T. Kato, S. Tabata, T. Noda and Y. Ohsumi, “Processing of ATG8s, Ubiquitin-Like Proteins, and Their Deconjugation by ATG4s Are essential for Plant Autophagy,” Plant Cell, Vol. 16, No. 11, 2004, pp. 2967-2983. doi:10.1105/tpc.104.025395
[24] S. Binder, “Branched-Chain Amino Acid Metabolism in Arabidopsis thaliana,” The Arabi-dopsis Book, Vol. 8, 2010, Article ID: e0137. doi:10.1199/tab.0137
[25] H. M. Lam, S. S. Peng and G. M. Coruzzi, “Metabolic Regulation of the Gene Encoding Glutamine-Dependent Asparagine Synthetase in Arabidopsis thaliana,” Plant Physiology, Vol. 106, No. 4, 1994, pp. 1347-1357. doi:10.1104/pp.106.4.1347

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.