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Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis

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Alternative pathway (AP) is involved in the tolerance of highland barley seedlings to the low-nitrogen stress by dissipating excessive reducing equivalents generated by photosynthesis and maintaining the cellular redox homeostasis.

Abstract

Low nitrogen (N) is a major limiting factor for plant growth and crop productivity. In this study, we investigated the roles of the alternative pathway (AP) in the tolerance of two barley seedlings, highland barley (Kunlun12) and barley (Ganpi6), to low-N stress. The results showed that the chlorophyll content and the fresh weight decreased more in Ganpi6 than those in Kunlun12 under low-N stress, suggesting that Kunlun12 has higher tolerance to low-N stress than Ganpi6. AP capacity was markedly induced by low-N stress; and it was higher in Kunlun12 than in Ganpi6. Comparatively, the cytochrome pathway capacity was not affected under all conditions. Western-blot analysis showed that the protein level of the alternative oxidase (AOX) increased under low-N stress in Kunlun12 but not in Ganpi6. Under low-N stress, the NAD(P)H content and the NAD(P)H to NAD(P)++NAD(P)H ratio in Ganpi6 increased more than those in Kunlun12. Furthermore, photosynthetic parameters (Fv/Fm, qP, ETR and Yield) decreased markedly and qN increased, indicating photoinhibition occurred in both barley seedlings, especially in Ganpi6. When AP was inhibited by salicylhydroxamic acid (SHAM), the NAD(P)H content and the NAD(P)H to NAD(P)++NAD(P)H ratio dramatically increased under all conditions, resulting in the marked accumulation of H2O2 and malondialdehyde in leaves of both barley seedlings. Meanwhile, the malate–oxaloacetate shuttle activity and the photosynthetic efficiency were further inhibited. Taken together, AP is involved in the tolerance of highland barley seedlings to low-N stress by dissipating excess reducing equivalents and maintaining the cellular redox homeostasis.

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Abbreviations

AOX:

Alternative oxidase

AP:

Alternative pathway

COX:

Cytochrome oxidase

CP:

Cytochrome pathway

H2O2 :

Hydrogen peroxide

Mal-OAA:

Malate–oxaloacetate

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

SHAM:

Salicylhydroxamic acid

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (31170225, 31201145), the Foundation of Science and Technology Program of Gansu Province (1208RJZA224), and Fundamental Research Funds for the Central Universities (lzujbky-2014-95, lzujbky-2013-bt05, lzujbky-2012-104).

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Correspondence to Yurong Bi.

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The authors declare that they have no conflict of interest. All authors have approved the manuscript for publication.

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Communicated by K. Chong.

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Wang, F., Wang, X., Zhao, C. et al. Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis. Plant Cell Rep 35, 317–328 (2016). https://doi.org/10.1007/s00299-015-1886-6

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