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Genetic reduction of inositol triphosphate (InsP3) increases tolerance of tomato plants to oxidative stress

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Abstract

Main conclusion

We demonstrate here that the reduction of InsP 3 , the key component of the phosphoinositol pathway, results in changes in ROS-scavenging machinery and, subsequently, increases the tolerance of tomato plants to light stress.

Different plant stress signaling pathways share similar elements and, therefore, ‘cross-talk’ between the various pathways can exist. Links between the phosphoinositol signaling pathway and light signaling were recently found. Tomato plants expressing InsP 5-ptase and exhibiting reduction in the level of inositol 1,4,5-triphosphate (InsP3) demonstrated enhanced tolerance to stress caused by continuous light exposure. To understand the molecular basis of observed stress tolerance in tomato lines with decreased amount of InsP3, we monitored the expression of enzymatic antioxidants as well as important factors in light signaling associated with non-enzymatic antioxidants (secondary metabolites). Here, we demonstrated that InsP 5-ptase transgenic plants accumulate less hydroxide peroxide and maintain higher chlorophyll content during stress caused by continuous light exposure. This observation can be explained by documented activation of multiple enzymatic antioxidants (LeAPX1, SICAT2, LeSOD) at levels of gene expression and enzymatic activities during continuous light exposure. In addition, we noticed the up-regulation of photoreceptors LePHYB and LeCHS1, key enzymes in flavonoid biosynthesis pathway, transcription factors LeHY5, SIMYB12, and early light-inducible protein (LeELIP) genes in transgenic tomato seedlings exposed to blue or red light. Our study confirmed the existence of a correlation between phosphoinositol signaling pathway modification, increased tolerance to stress caused by continuous light exposure, activation of ROS-scavenging enzymes, and up-regulation of molecular activators of non-enzymatic antioxidants in InsP 5-ptase expressing tomato lines.

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Abbreviations

InsP3 :

Inositol 1,4,5-triphosphate

InsP 5-ptase:

Inositol trisphosphate 5 phosphatase

SOD:

Superoxide dismutase

CAT:

Catalase

APX:

Ascorbate peroxidase

LeCHS1:

Lycopersicon esculentum chalcone synthase

LeHY5:

Lycopersicon esculentum long hypocotyl 5 transcription factor

LePHYB:

Lycopersicon esculentum photochrome B

SICRY1:

Solanum lycopersicum cryptochrome 1

LeELIP:

Lycopersicon esculentum early light-inducible protein

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Acknowledgments

Funding from EPSCoR-NSF-P3 Center (Grant P3-202 to MVK) and NASA-EPSCoR (Grant to MVK) is highly appreciated. Authors thank EPSCoR-NSF-P3 Center, Graduate Institute of Technology and College of Science, UALR for providing graduate assistantship to Mohammad Alimohammadi. We are grateful to Dr. Julian Post for designing and building of LED light boxes used for light exposure experiment. The editorial assistance of Dr. Marinelle Ringer is also acknowledged.

Conflict of interest

The authors declare no competing financial interests.

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Authors and Affiliations

  1. Department of Biology, University of Arkansas at Little Rock, Little Rock, USA

    Mohammad Alimohammadi, Mohamed H. Lahiani & Mariya V. Khodakovskaya

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  1. Mohammad Alimohammadi
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  2. Mohamed H. Lahiani
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  3. Mariya V. Khodakovskaya
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Correspondence to Mariya V. Khodakovskaya.

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Alimohammadi, M., Lahiani, M.H. & Khodakovskaya, M.V. Genetic reduction of inositol triphosphate (InsP3) increases tolerance of tomato plants to oxidative stress. Planta 242, 123–135 (2015). https://doi.org/10.1007/s00425-015-2289-1

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