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Relationship Between Carbon Mobilization and Root Growth Measured by Carbon-11 Tracer in Arabidopsis Starch Mutants

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Abstract

Experiments designed to quantify the physiological and metabolic status of Arabidopsis thaliana seedlings across their photoperiod used wild-type (Col-0) and genotypes deficient in starch biosynthesis (adg1-1, pgm-1) and in starch degradation (sex1-1) in combination with radioactive 11CO2 tracer. Measurements of root allocation and root exudation of 11C-photosynthates were conducted at 1 and 8 h into a 10-h photoperiod. Additionally, bioassays conducted on leaflets provided a measure of ‘new’ carbon partitioning (as 11C) into structural and non-structural carbohydrates. As expected, starch biosynthesis increased across the photoperiod for Col-0 controls. This increase was correlated with systematic decreases in soluble sugar synthesis and sink allocation across the photoperiod. We showed that this was a causal effect, which could be eliminated in the adg1-1 and pgm-1 mutants that were deficient in starch biosynthesis. Furthermore, these genotypes exhibited systematically higher levels of soluble sugars and sink allocation relative to Col-0 and sex1-1, which resulted in very different root growth traits including (i) increased root area balanced by shorter primary roots; (ii) increased number of lateral roots; and (iii) decreased root gravitropism. These differences in growth traits were correlated with higher observed levels of root auxin in these genotypes and to lower starch levels in their root tips. In a broader context, we find that carbon storage in the aboveground tissues can strongly influence root growth and root architecture belowground.

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Acknowledgements

This article has been authored under contracts DE-SC0012704 in support of the Radiochemistry Program with the U.S. Department of Energy (DOE), which supported R. Ferrieri and M. Schueller in this effort. A DOE training grant through the University of Missouri (Grant No. DE-SC0002040) supported L. Song, and the DOE SULI Program supported B. Agtuca on this project. We also would like to acknowledge the MU Molecular Cytology Research Core Facility for helping with the microscopic images of root tip starch granules.

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Authors and Affiliations

  1. Department of Chemistry, University of Missouri, Columbia, MO, 65211, USA

    Lihui Song, Michael J. Schueller, Silvia S. Jurisson & Richard A. Ferrieri

  2. Division of Plant Sciences, Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA

    Beverly Agtuca

  3. Missouri Research Reactor Center, University of Missouri, 1513 Research Park Drive, Columbia, MO, 65211, USA

    Michael J. Schueller & Richard A. Ferrieri

  4. Division of Plant Sciences and Biochemistry, Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA

    Gary Stacey

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  1. Lihui Song
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Contributions

LS and BA conducted the laboratory tracer studies. MJS produced the isotope and assisted with the design of plant tracer boxes. SSJ and GS helped with data interpretation and with manuscript editing. RAF designed the tracer studies, managed the workflow, interpreted the data, and wrote the manuscript.

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Correspondence to Richard A. Ferrieri.

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Supplemental Figure S1

. Panel a: Petri dish showing growth template for A. thaliana seedlings in Gelzan™ media. Panel b: experimental setup for administering 11CO2 tracer to Petri dish grown A. thaliana seedlings. Panel c: rack setup for assembling Eppendorf tube grown A. thaliana seedlings – note placement of plant less control tubes. Panel d: transparent cover is affixed to the rack enabling uniform introduction of 11CO2 tracer. (TIF 978 KB)

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Song, L., Agtuca, B., Schueller, M.J. et al. Relationship Between Carbon Mobilization and Root Growth Measured by Carbon-11 Tracer in Arabidopsis Starch Mutants. J Plant Growth Regul 38, 164–179 (2019). https://doi.org/10.1007/s00344-018-9824-9

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