Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-06-08T07:44:41.568Z Has data issue: false hasContentIssue false
  • English
  • Français

Different respiration metabolism between mycorrhizal and non-mycorrhizal rice under low-temperature stress: a cry for help from the host

Published online by Cambridge University Press:  20 May 2014

Z. LIU ,
Y. LI ,
J. WANG ,
X. HE  and
C. TIAN
Z. LIU
Affiliation:
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin 130102, People's Republic of China University of the Chinese Academy of Sciences, Beijing 100049, People's Republic of China
Y. LI
Affiliation:
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin 130102, People's Republic of China University of the Chinese Academy of Sciences, Beijing 100049, People's Republic of China
J. WANG
Affiliation:
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin 130102, People's Republic of China
X. HE
Affiliation:
Laboratory of Urban Forest and Wetland, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin 130102, People's Republic of China
C. TIAN*
Affiliation:
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin 130102, People's Republic of China
*
*To whom all correspondence should be addressed. Email: tiancj@neigae.ac.cn
Get access Rights & Permissions [Opens in a new window]

Summary

Low-temperature stress is an important environmental factor that severely disrupts plant respiration but can be alleviated by symbiotic arbuscular mycorrhizal fungi (AMF). In the current study, a pot experiment was performed to determine changes in the respiratory metabolic capacity of mycorrhizal rice (Oryza sativa) under low-temperature stress. The results demonstrated that low temperature might accelerate the biosynthesis of strigolactone in mycorrhizal rice roots by triggering the expression of genes for the synthesis of strigolactone, which acted as a host stress response signal. In addition, AMF prompted the host tricarboxylic acid (TCA) cycle by enhancing pyruvate metabolism, up-regulating the expression of genes of the TCA cycle under low-temperature stress and affecting the electron transport chain. The alternative oxidase pathway might be the main electron transport pathway in non-mycorrhizal rice under stress, while the cytochrome c oxidase (COX) pathway might be the predominant pathway in arbuscular mycorrhizal symbiosis. Mycorrhizal rice also had higher adenosine triphosphate production to maintain the natural status of respiration under stress conditions, which resulted in improved root growth status and alleviated low-temperature stress.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 153 , Issue 4 , May 2015 , pp. 602 - 614
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abiko, T., Obara, M., Ushioda, A., Hayakawa, T., Hodges, M. & Yamaya, T. (2005). Localization of NAD-isocitrate dehydrogenase and glutamate dehydrogenase in rice roots: candidates for providing carbon skeletons to NADH-glutamate synthase. Plant and Cell Physiology 46, 1724–1734.Google Scholar
Akiyama, K. & Hayashi, H. (2006). Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Annals of Botany 97, 925–931.Google Scholar
Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P. & Al-Babili, S. (2012). The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335, 1348–1351.Google Scholar
Aliverdieva, D. A., Mamaev, D. V., Lagutina, L. S. & Sholtz, K. F. (2006). Specific features of changes in levels of endogenous respiration substrates in Saccharomyces cerevisiae cells at low temperature. Biochemistry 71, 39–45.Google Scholar
Aroca, R., Ruiz-Lozano, J. M., Zamarreno, A. M., Paz, J. A., Garcia-Mina, J. M., Pozo, M. J. & López-Ráez, J. A. (2013). Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. Journal of Plant Physiology 170, 47–55.Google Scholar
Atkin, O. K., Sherlock, D., Fitter, A. H., Jarvis, S., Hughes, J. K., Campbell, C., Hurry, V. & Hodge, A. (2009). Temperature dependence of respiration in roots colonized by arbuscular mycorrhizal fungi. New Phytologist 182, 188–199.Google Scholar
Atkinson, L. J., Hellicar, M. A., Fitter, A. H. & Atkin, O. K. (2007). Impact of temperature on the relationship between respiration and nitrogen concentration in roots: an analysis of scaling relationships, Q10 values and thermal acclimation ratios. New Phytologist 173, 110–120.Google Scholar
Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P. & Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8, 443–449.Google Scholar
Campos-Soriano, L., Garcia-Martinez, J. & San Segundo, B. (2012). The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Molecular Plant Pathology 13, 579–592.Google Scholar
de Saint Germain, A., Bonhomme, S., Boyer, F. D. & Rameau, C. (2013). Novel insights into strigolactone distribution and signalling. Current Opinion in Plant Biology 16, 583–589.Google Scholar
Dinakar, C., Abhaypratap, V., Yearla, S. R., Raghavendra, A. S. & Padmasree, K. (2010 a). Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Planta 231, 461–474.Google Scholar
Dinakar, C., Raghavendra, A. S. & Padmasree, K. (2010 b). Importance of AOX pathway in optimizing photosynthesis under high light stress: role of pyruvate and malate in activating AOX. Physiologia Plantarum 139, 13–26.Google Scholar
Fernie, A. R., Carrari, F. & Sweetlove, L. J. (2004). Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology 7, 254–261.Google Scholar
Florez-Sarasa, I., Flexas, J., Rasmusson, A. G., Umbach, A. L., Siedow, J. N. & Ribas-Carbo, M. (2011). In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant Cell & Environment 34, 1373–1383.Google Scholar
Fuentes, R. G., Baltazar, A. M., Merca, F. E., Ismail, A. M. & Johnson, D. E. (2010). Morphological and physiological responses of lowland purple nutsedge (Cyperus rotundus L.) to flooding. AoB Plants 10, plq010. doi: 10.1093/aobpla/plq010.Google Scholar
Gavito, M. E. & Azcon-Aguilar, C. (2012). Temperature stress in arbuscular mycorrhizal fungi: a test for adaptation to soil temperature in three isolates of Funneliformis mosseae from different climates. Agricultural and Food Science 21, 2–11.CrossRefGoogle Scholar
Govindarajulu, M., Pfeffer, P. E., Jin, H., Abubaker, J., Douds, D. D., Allen, J. W., Bucking, H., Lammers, P. J. & Shachar-Hill, Y. (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823.Google Scholar
Hughes, J. K., Hodge, A., Fitter, A. H. & Atkin, O. K. (2008). Mycorrhizal respiration: implications for global scaling relationships. Trends in Plant Science 13, 583–588.Google Scholar
Jakobsen, I. & Rosendahl, L. (1990). Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115, 77–83.Google Scholar
Kaklewski, K., Nowak, J. & Ligocki, M. (2008). Effects of selenium content in green parts of plants on the amount of ATP and ascorbate-glutathione cycle enzyme activity at various growth stages of wheat and oilseed rape. Journal of Plant Physiology 165, 1011–1022.CrossRefGoogle ScholarPubMed
Karasawa, T., Hodge, A. & Fitter, A. H. (2012). Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant, Cell & Environment 35, 819–828.Google Scholar
Kim, B. R., Nam, H. Y., Kim, S. U., Kim, S. I. & Chang, Y. J. (2003). Normalization of reverse transcription quantitative-PCR with housekeeping genes in rice. Biotechnology Letters 25, 1869–1872.Google Scholar
Kurimoto, K., Millar, A. H., Lambers, H., Day, D. A. & Noguchi, K. (2004). Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant and Cell Physiology 45, 1015–1022.Google Scholar
Labate, C. A. & Leegood, R. C. (1989). Influence of low temperature on respiration and contents of phosphorylated intermediates in darkened barley leaves. Plant Physiology 91, 905–910.Google Scholar
Lee, B. R., Muneer, S., Avice, J. C., Jung, W. J. & Kim, T. H. (2012 a). Mycorrhizal colonisation and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 22, 525–534.Google Scholar
Lee, B. R., Muneer, S., Jung, W. J., Avice, J. C., Ourry, A. & Kim, T. H. (2012 b). Mycorrhizal colonization alleviates drought-induced oxidative damage and lignification in the leaves of drought-stressed perennial ryegrass (Lolium perenne). Physiologia Plantarum 145, 440–449.Google Scholar
Li, C. R., Liang, D. D., Li, J., Duan, Y. B., Li, H., Yang, Y. C., Qin, R. Y., Li, L., Wei, P. C. & Yang, J. B. (2013). Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice ALTERNATIVE OXIDASE 1 genes. Plant, Cell & Environment 36, 775–788.Google Scholar
Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J. & Wang, Y. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. The Plant Cell 21, 1512–1525.Google Scholar
Liu, Z. L., Li, Y. J., Hou, H. Y., Zhu, X. C., Rai, V., He, X. Y. & Tian, C. J. (2013). Differences in the arbuscular mycorrhizal fungi-improved rice resistance to low temperature at two N levels: aspects of N and C metabolism on the plant side. Plant Physiology and Biochemistry 71, 87–95.Google Scholar
López-Ráez, J. A., Pozo, M. J. & García-Garrido, J. M. (2011). Strigolactones: a cry for help in the rhizosphere. Botany 89, 513–522.Google Scholar
Matusova, R., Rani, K., Verstappen, F. W. A., Franssen, M. C. R., Beale, M. H. & Bouwmeester, H. J. (2005). The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiology 139, 920–934.Google Scholar
Maxwell, D. P., Wang, Y. & McIntosh, L. (1999). The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences of the United States of America 96, 8271–8276.Google Scholar
Meier, U. (Ed.) (2001). Growth Stages of Mono- and Dicotyledonous Plants, 2nd edn, pp. 19–23. BBCH Monograph. Braunschweig: Federal Biological Research Centre for Agriculture and Forestry.Google Scholar
Nelson, D. W. & Sommers, L. E. (1973). Determination of total nitrogen in plant material. Agronomy Journal 65, 109–112.Google Scholar
Nunes-Nesi, A., Sulpice, R., Gibon, Y. & Fernie, A. R. (2008). The enigmatic contribution of mitochondrial function in photosynthesis. Journal of Experimental Botany 59, 1675–1684.Google Scholar
Obata, T. & Fernie, A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences 69, 3225–3243.Google Scholar
Oliver, S. N., Lunn, J. E., Urbanczyk-Wochniak, E., Lytovchenko, A., van Dongen, J. T., Faix, B., Schmalzlin, E., Fernie, A. R. & Geigenberger, P. (2008). Decreased expression of cytosolic pyruvate kinase in potato tubers leads to a decline in pyruvate resulting in an in vivo repression of the alternative oxidase. Plant Physiology 148, 1640–1654.CrossRefGoogle Scholar
Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6, 763–775.CrossRefGoogle ScholarPubMed
Pastore, D., Trono, D., Laus, M. N., Di Fonzo, N. & Passarella, S. (2001). Alternative oxidase in durum wheat mitochondria. Activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant and Cell Physiology 42, 1373–1382.Google Scholar
Perez-Moreno, J. & Read, D. J. (2001). Nutrient transfer from soil nematodes to plants: a direct pathway provided by the mycorrhizal mycelial network. Plant Cell & Environment 24, 1219–1226.Google Scholar
Phillips, J. M. & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.Google Scholar
Requena, N., Serrano, E., Ocon, A. & Breuninger, M. (2007). Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68, 33–40.Google Scholar
Ribas-Carbo, M., Aroca, R., Gonzalez-Meler, M. A., Irigoyen, J. J. & Sanchez-Diaz, M. (2000). The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiology 122, 199–204.Google Scholar
Ruyter-Spira, C., Al-Babili, S., van der Krol, S. & Bouwmeester, H. (2013). The biology of strigolactones. Trends in Plant Science 18, 72–83.Google Scholar
Trouvelot, A., Fardeau, J. C., Plenchette, C., Gianinazzi, S. & Gianinazzapearson, V. (1986). Nutritional balance and symbiotic expression in mycorrhizal wheat. Physiologie Vegetale 24, 300.Google Scholar
Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N. & Yamaguchi, S. (2010). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant and Cell Physiology 51, 1118–1126.Google Scholar
Valentine, A. J. & Kleinert, A. (2007). Respiratory responses of arbuscular mycorrhizal roots to short-term alleviation of P deficiency. Mycorrhiza 17, 137–143.Google Scholar
Vanlerberghe, G. C., Cvetkovska, M. & Wang, J. (2009). Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiologia Plantarum 137, 392–406.Google Scholar
Wang, J., Rajakulendran, N., Amirsadeghi, S. & Vanlerberghe, G. C. (2011). Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiologia Plantarum 142, 339–351.Google Scholar
Winer, J., Jung, C. K., Shackel, I. & Williams, P. M. (1999). Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Analytical Biochemistry 270, 41–49.Google Scholar
Wintermans, J. F. & de Mots, A. (1965). Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochimica et Biophysica Acta 109, 448–453.Google Scholar
Zhang, L. T., Zhang, Z. S., Gao, H. Y., Meng, X. L., Yang, C., Liu, J. G. & Meng, Q. W. (2012). The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biology 12, 40. doi: 10.1186/1471-2229-12-40.Google Scholar
Zhao, X. & Fitzgerald, M. (2013). Climate change: implications for the yield of edible rice. PLoS One 8(6), e66218. doi: 10.1371/journal.pone.0066218.Google Scholar