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. 2013 Feb 5;110(6):2407-12.
doi: 10.1073/pnas.1217024110. Epub 2013 Jan 23.

Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes

Zhilong Bao  1 , Huijun Yang, Jian Hua
Affiliations

Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes

Zhilong Bao et al. Proc Natl Acad Sci U S A. .

Abstract

The Arabidopsis gene OSD1 (Omission of the Second Division) and its homolog UVI4 (UV-B-Insensitive 4) are negative regulators of anaphase-promoting complex/cyclosome (APC/C), a multisubunit ubiquitin E3 ligase that regulates the progression of cell cycles. Here we report the isolation of an activation tagging allele of OSD1 as an enhancer of a mutant of BON1 (BONZAI1), a negative regulator of plant immunity. Overexpression of OSD1 and UVI4 each leads to enhanced immunity to a bacterial pathogen, which is associated with increased expression of disease resistance (R) genes similar to the animal NOD1 receptor-like immune receptor genes. In addition, the reduction of function of one subunit of the APC complex APC10 exhibited a similar phenotype to that of overexpression of OSD1 or UVI4, indicating that altered APC function induces immune responses. Enhanced immune response induced by OSD1 overexpression is dependent on CYCB1;1, which is a degradation target of APC/C. It is also associated with up-regulation of R genes and is dependent on the R gene SNC1 (Suppressor of npr1-1, constitutive 1). Taken together, our findings reveal an unexpected link between cell cycle progression and plant immunity, suggesting that cell cycle misregulation could have an impact on expression of genes, including R genes, in plant immunity.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
ebo30 mutation enhances the bon1-2 phenotype. (A) Morphology of bon1-2, bon1-2 ebo30, ebo30, and bon1-2 ebo30 eds1 plants grown at 22 °C for 4 wk. (B) Growth of virulent bacterial pathogen Pst DC3000 in Ws, bon1-2, ebo30, and bon1-2 ebo30 at day 0 and day 4 after inoculation. The asterisk indicates a statistically significant difference from Col-0 determined by the Student t test (P < 0.05). (C and D) Expression of PR1 (C) and R genes (D) in Ws, bon1-2, and bon1-2 ebo30 were analyzed by RNA blotting. rRNAs were used as loading controls. (E) Diagram of the genomic region around the ebo30 mutation. The activation tag is inserted in At3g57870, which is adjacent to At3g57860. (F) Expression of At3g57860 in bon1-2 ebo30 analyzed by RNA blotting.
Fig. 2.
Fig. 2.
Overexpression of OSD1 and UVI4 confers enhanced disease resistance. (A) Growth phenotypes of OSD1-OE and UVI4-OE plants before bolting. A representative line from each is shown. (B) Growth of Pst DC3000 in OSD1-OE and UVI4-OE plants at day 0 and day 3 after inoculation. The asterisk indicates a statistically significant difference from Col-0 determined by the Student t test (P < 0.05). (C) PR1 expression analyzed by RNA blots for overexpression lines at age 3 wk. (D) Growth phenotypes of OSD1-OE in Col-0 and pad4. (E) Growth phenotypes of the same UVI4-OE transgenic line in pad4 and pad4/+ (from a cross to the WT Col-0). (F) Growth phenotypes of overexpression lines at 22 °C and 28 °C. The white bars in whole plant images represent 1 cm in all figures.
Fig. 3.
Fig. 3.
Effects on defense responses from the loss of UVI4 or OSD1 function. (A) Growth of Pst DC3000 in uvi4 and osd1-2C at day 0 and day 3 after inoculation. In this test, uvi4 was not significantly different from the WT. (B) Growth of Pst DC3000 in uvi4 at day 0 and day 3 after the inoculation. In this test, uvi4 was significantly more resistant to pathogen compared with WT. The asterisk indicates a statistically significant difference from Col-0 determined by the Student t test (P < 0.05).
Fig. 4.
Fig. 4.
Perturbation of APC/C and its activators affects defense responses. (A) Interaction of APC8 with UVI4 and OSD1 assayed by yeast two-hybrid. Shown are serial dilutions of yeast cells containing the fusion proteins with GAL4 AD (activation domain) and GAL4 BD (DNA binding) plated on interaction selection plates. (B) Growth phenotypes of APC10RNAi plants under 12 h-light per day conditions for 4 wk (C and D) Growth of Pst DC3000 in the APC10RNAi line (C), css52a1-1 (D), and css52b-1 (D) compared with WT Col-0 at 0 and 3 d after inoculation. The asterisks indicate statistically significant differences from Col-0 determined by the Student t test (P < 0.05).
Fig. 5.
Fig. 5.
Defense response activation in osd1-4C is dependent on CYCB1;1. (A) Expression of CYCB1;1 and OSD1 in Col-0, cycb1;1, osd1-4C, and osd1-4C cycb1;1 analyzed by RT-PCR. (B) Growth phenotypes of Col-0, cycb1;1, osd1-4C, and osd1-4C cycb1;1. (C) Growth of Pst DC3000 in the above genotypes. The asterisk indicates a statistically significant difference from Col-0 determined by the Student t test (P < 0.05). (D) qRT-PCR analysis of SNC1 expression in the above genotypes. Error bar indicates SD determined from three measurements.
Fig. 6.
Fig. 6.
Enhanced disease resistance in osd1-4C is dependent on SNC1. (A) Growth phenotypes of Col-0, snc1-11, osd1-4C, and osd1-4C snc1-11. (B) Growth of Pst DC3000 in the above genotypes. The asterisk indicates a statistically significant difference from Col-0 determined by the Student t test (P < 0.05).
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