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Exogenous Glucose Mediates the Regulation of Root Morphology and Carbon–Nitrogen Metabolism by Indole-3-Acetic Acid (IAA) in Malus baccata (L.) Borkh. in Soil with Low Organic Carbon Content

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Abstract

The effects of an exogenous organic carbon source (i.e., glucose) and indole-3-acetic acid (IAA) on root architecture and carbon–nitrogen (C–N) metabolism of apple rootstock were evaluated under soil organic matter (SOM)-restricted conditions. Malus baccata (L.) Borkh. seedlings were exposed to 1.5 g kg−1 glucose (GLC), 0.09 g kg−1 IAA, 0.06 g kg−1 2,3,5-triiodobenzoic acid (TIBA, a widely used auxin polar transport inhibitor), GLC + IAA, or GLC + TIBA for 30 days. Both GLC and IAA promoted root architecture and growth by regulating SHY2, SHR, ALF4, and LBD11. They also enhanced C–N metabolism, and accelerated nitrate transformation to amino acids. In contrast, TIBA reduced endogenous IAA content in root and inhibited plant growth and C–N metabolism by downregulating expression of auxin polar transport genes, although auxin biosynthesis genes were induced. These adverse effects could be alleviated in GLC + TIBA, which exhibited higher endogenous IAA content in root than TIBA-treated seedlings alone, due to the upregulated expression of auxin biosynthesis genes (YUCCA8, TAR2, TAA1, and CYP79B3) and polar transport genes (PIN1, AUX1, and LAX2). In addition, the enhanced transcription and activities of enzymes involved in C metabolism (PEPC, NADP-ME, and NADP-ICDH) could provide more organic acids, adenosine triphosphate (ATP), and energy charge for N metabolism in roots under GLC + TIBA than in roots under TIBA. The induced NR, GS, NADH-GDH, NADH-GOGAT activities and mRNA levels of genes involved in N metabolism indicated the higher N assimilation ability in roots under GLC + TIBA than in roots under TIBA alone. In conclusion, exogenous glucose-mediated IAA biosynthesis and polar transport regulates root architecture and C–N metabolism of M. baccata (L.) Borkh. under low-SOM conditions.

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Acknowledgements

This study was funded by the National Key Research and Development Program of China (Grant No. 2016YFD0201115), the China Agriculture Research System (CARS-27), and the Program for High-level Talent of Shenyang city (RC170201, 18-013-0-77).

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  1. College of Horticulture, Shenyang Agricultural University, No. 120 Dongling Road, Shenyang, 110866, Liaoning, People’s Republic of China

    Dongmei Lang, Deguo Lyu, Zitan Zhu & Sijun Qin

  2. Key Lab of Fruit Quality Development and Regulation of Liaoning Province, Shenyang, 110866, Liaoning, People’s Republic of China

    Deguo Lyu & Sijun Qin

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  1. Dongmei Lang
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  2. Deguo Lyu
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DL and SQ conceived and designed the experiment. DL and ZZ performed the experiments. DL analyzed the data. DL, DL, and SQ wrote the paper. All authors gave their final approval of the submitted and published versions.

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344_2019_10005_MOESM1_ESM.pptx

Supplementary material 1—Effects of glucose and/or IAA treatment on the ZT content in the root of Malus baccata (L.) Borkh. Values represent means ± SDs (n = 3). Different letters indicate significant differences at p < 0.05 according to Turkey’s test. IAA, 0.09 g·kg-1 indoleacetic acid; TIBA, 0.06 g·kg-1 2,3,5-triiodobenzoic acid; GLC, 1.50 g·kg-1 glucose; GLC+IAA, 1.50 g·kg-1 glucose and 0.09 g·kg-1 indoleacetic acid; GLC+TIBA, 1.50 g·kg-1 glucose and 0.06 g·kg-1 2,3,5-triiodobenzoic acid (PPTX 59 kb)

344_2019_10005_MOESM2_ESM.pptx

Supplementary material 2—Effects of glucose and/or IAA treatment on the IAA content in soil. Values represent means ± SDs (n = 3). Different letters indicate significant differences at p < 0.05 according to Turkey’s test. IAA, 0.09 g·kg-1 indoleacetic acid; TIBA, 0.06 g·kg-1 2,3,5-triiodobenzoic acid; GLC, 1.50 g·kg-1 glucose; GLC+IAA, 1.50 g·kg-1 glucose and 0.09 g·kg-1 indoleacetic acid; GLC+TIBA, 1.50 g·kg-1 glucose and 0.06 g·kg-1 2,3,5-triiodobenzoic acid (PPTX 83 kb)

344_2019_10005_MOESM3_ESM.pptx

Supplementary material 3—Effects of glucose and/or IAA treatment on soil organic matter and available nutrient contents. Values represent means ± SDs (n = 3). Different letters indicate significant differences at p < 0.05 according to Turkey’s test. IAA, 0.09 g·kg-1 indoleacetic acid; TIBA, 0.06 g·kg-1 2,3,5-triiodobenzoic acid; GLC, 1.50 g·kg-1 glucose; GLC+IAA, 1.50 g·kg-1 glucose and 0.09 g·kg-1 indoleacetic acid; GLC+TIBA, 1.50 g·kg-1 glucose and 0.06 g·kg-1 2,3,5-triiodobenzoic acid (PPTX 196 kb)

Supplementary material 4—The scan images of roots under glucose and/or IAA treatment (PPTX 1344 kb)

Supplementary material 5—Gene-specific primers used for quantitative real-time PCR (DOCX 16 kb)

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Lang, D., Lyu, D., Zhu, Z. et al. Exogenous Glucose Mediates the Regulation of Root Morphology and Carbon–Nitrogen Metabolism by Indole-3-Acetic Acid (IAA) in Malus baccata (L.) Borkh. in Soil with Low Organic Carbon Content. J Plant Growth Regul 38, 1598–1615 (2019). https://doi.org/10.1007/s00344-019-10005-2

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