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. 2008 Jan;20(1):228-40.
doi: 10.1105/tpc.107.055657. Epub 2008 Jan 11.

Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice

Xinhua Ding  1 , Yinglong Cao, Liling Huang, Jing Zhao, Caiguo Xu, Xianghua Li, Shiping Wang
Affiliations

Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice

Xinhua Ding et al. Plant Cell. 2008 Jan.

Abstract

New evidence suggests a role for the plant growth hormone auxin in pathogenesis and disease resistance. Bacterial infection induces the accumulation of indole-3-acetic acid (IAA), the major type of auxin, in rice (Oryza sativa). IAA induces the expression of expansins, proteins that loosen the cell wall. Loosening the cell wall is key for plant growth but may also make the plant vulnerable to biotic intruders. Here, we report that rice GH3-8, an auxin-responsive gene functioning in auxin-dependent development, activates disease resistance in a salicylic acid signaling- and jasmonic acid signaling-independent pathway. GH3-8 encodes an IAA-amino synthetase that prevents free IAA accumulation. Overexpression of GH3-8 results in enhanced disease resistance to the rice pathogen Xanthomonas oryzae pv oryzae. This resistance is independent of jasmonic acid and salicylic acid signaling. Overexpression of GH3-8 also causes abnormal plant morphology and retarded growth and development. Both enhanced resistance and abnormal development may be caused by inhibition of the expression of expansins via suppressed auxin signaling.

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Figures

Figure 1.
Figure 1.
Expression of the GH3-8 Gene and Phenotypes of GH3-8–Overexpressing Plants (Mudanjiang 8 Is the Wild Type). (A) GH3-8 expression in C101LAC (donor of GH3-8; D), wild-type, and T0 transgenic plants (D25UM8) detected by RNA gel blot analysis. (B) Growth of PXO61 in leaves of GH3-8–overexpressing (D25UM8-2) and wild-type plants. The bacterial population was determined from three leaves at each time point by counting colony-forming units (cfu) (Sun et al., 2004). 0 day, 2 h after bacterial inoculation. Each point represents a mean ± sd. (C) Transgenic plants grown on rooting medium in the absence of auxin. Left, GH3-8–overexpressing plant; right, negative transgenic plant. (D) GH3-8–overexpressing plants grown on rooting medium supplemented with 0.3 mg/L 2,4,5-T for 10 d. (E) Adult plants grown in the field. From left to right are the most stunted T0 plant (D25UM8-2), a moderate dwarf T0 plant (D25UM8-28), and the wild type (Mudanjiang 8). (F) and (G) T1 plants from transgenic plant D25UM8-27 that overexpressed GH3-8. Left, abnormal T1 plant; right, normal T1 plant.
Figure 2.
Figure 2.
Function of GH3-8. (A) Quantification of free IAA and IAA–amino acid conjugates (IAA-Asp and IAA-Ala) in the leaves of GH3-8–overexpressing plants (D25UM8-2, -28, and -33) and a GH3-8–knockout plant (03Z11EV19; M) at the booting stage. FW, fresh weight; W1, wild-type Mudanjiang 8 for GH3-8–overexpressing plants; W2, wild-type Zhonghua 11 for the GH3-8–knockout plant. Bars represent means (three replicates) ± sd. Asterisks indicate that a significant difference (P < 0.05) was detected between GH3-8–overexpressing and W1 plants. (B) HPLC analysis of amino acid conjugates of IAA synthesized by recombinant GH3-8 protein in different time courses. Standard IAA (peak a), IAA-Asp (peak b), and IAA-Ala (peak c) were bought from Sigma-Aldrich. ck, proteins from E. coli transferred with the null vector PET28a.
Figure 3.
Figure 3.
Effect of IAA on the Development of Disease and Expression Patterns of Auxin Synthesis–Related Genes. (A) Exogenous application of IAA or 2,4-D increased lesion area in resistant rice lines Minghui 63 and Rb17 after PXO61 inoculation. Mudanjiang 8 was not treated with 100 μM 2,4-D. Bars represent means (five replicates) ± sd. Asterisks indicate that a significant difference (P < 0.05) was detected between IAA- or 2,4-D–treated plants and untreated (ck) plants. (B) Bacterial infection induced the accumulation of free IAA and IAA-Asp in both GH3-8–overexpressing (D25UM-28) and wild-type (Mudanjiang 8) plants. Approximately 6-cm-long leaf fragments right next to the inoculation site were used for the analysis. Each point represents a mean (three replicates) ± sd. 0 h, immediately after inoculation with PXO61. FW, fresh weight. (C) Expression patterns of IAA synthesis–related genes on PXO61 infection in Mudanjiang 8. The expression level of each gene was calculated relative to that in the plants immediately after inoculation (0 h). Each point represents a mean (three replicates) ± sd.
Figure 4.
Figure 4.
Expression of Auxin Signaling–Related Genes Was Influenced by IAA and Pathogen Infection. Mudanjiang 8 is the wild type. Each point represents a mean (three replicates) ± sd. (A) Expression of Aux/IAA and ARF gene families was influenced after IAA treatment (10 μM) in GH3-8–overexpressing (D25UM8-2) and wild-type plants. The expression level of each gene was calculated relative to that in untreated (ck) wild-type plants. (B) Both resistant and susceptible reactions influenced the expression of GH3-8 as well as IAA and ARF genes. Plants were inoculated with Xoo strain PXO61. 0 h (control), immediately after inoculation. The expression level of each gene was calculated relative to that in control wild-type plants. (C) Both resistant and susceptible reactions influenced the accumulation of free IAA and IAA-Asp. 0 h (control), immediately after inoculation. Each point represents a mean (three replicates) ± sd. FW, fresh weight.
Figure 5.
Figure 5.
Overexpression of GH3-8 Suppresses the Accumulation of SA and JA and the Expression of Defense-Responsive Genes Functioning in SA- and JA-Dependent Pathways. Bars represent means (three replicates) ± sd. Asterisks indicate that a significant difference (P < 0.05) was detected between GH3-8–overexpressing plants and wild-type plants. (A) Expression patterns of defense-responsive genes. (B) SA and conjugated SA levels in rice leaves. FW, fresh weight. (C) JA levels in rice leaves.
Figure 6.
Figure 6.
IAA and Bacteria Influence the Expression of Expansin Genes. Bars represent means (three replicates) ± sd. Asterisks indicate that a significant difference (P < 0.05) was detected between GH3-8–overexpressing plants or R-gene–carrying transgenic plants and wild-type (Mudanjiang 8) plants. (A) Expression patterns of expansin genes in GH3-8–overexpressing (D25UM8-2) or wild-type plants after IAA treatment. The plants were treated with IAA for 30, 60, or 120 min. ck, without treatment. (B) Pathogen infection influenced the expression of expansin genes in both R gene–carrying (D49O and Rb49) and wild-type plants. Plants were inoculated with PXO61 for 0 (measured immediately after inoculation), 2, 6, or 12 h.
Figure 7.
Figure 7.
Overexpression of Expansin Genes (EXPA1, EXPA5, and EXPA10) Was Associated with Increased Susceptibility to Xoo Strain PXO61. Bars represent means (three replicates) ± sd. Asterisks indicate that a significant difference (P < 0.05) was detected between transgenic plants (OVEXPA1-, OVEXPA5-, and OVEXPA10-) and wild-type Zhonghua 11 (W).
Figure 8.
Figure 8.
Expression Pattern of GH3-8. (A) GH3-8 had different expression levels in various tissues analyzed by qRT-PCR. Tissues were obtained from rice var Minghui 63. Column 1, leaf; column 2, sheath; column 3, stamen; column 4, pistil; column 5, root; column 6, young panicle (3- to 5-cm stage). Bars represent means (three replicates) ± sd. (B) PGH3-8:GUS expression in transgenic rice plants. Blue indicates the expression of GUS. M, mesophyll cell; P, parenchyma cells; V, vascular elements. Bar = 30 μm.
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