Yiwen Deng, Keran Zhai,Zhen Xie, Dongyong Yang, Xudong Zhu, Junzhong Liu, Xin Wang, Peng Qin, Yuanzhu Yang, Guomin Zhang, Qun Li, Jianfu Zhang, Shuangqing Wu, Joëlle Milazzo, Bizeng Mao, Ertao Wang, Huaan Xie, Didier Tharreau, Zuhua He
Science Feb 2 2017 (10.1126/science.aai8898 (2017)
Crop breeding aims to balance disease resistance with yield, however single resistance ( R ) genes can lead to resistance breakdown and R gene pyramiding may impact growth fitness. Here we report that the rice Pigm locus contains a cluster of genes encoding nucleotide-binding leucine-rich repeat (NLR) receptors that confer durable resistance to the fungus Magnaporthe oryzae without yield penalty. In the cluster, PigmR confers broad-spectrum resistance, whereas PigmS competitively attenuates PigmR homodimerization to suppress resistance. PigmS expression, and thus PigmR -mediated resistance, are subjected to tight epigenetic regulation.
PigmS increases seed production to counteract the yield cost induced by PigmR . Therefore, our study reveals a mechanism balancing high disease resistance and yield through epigenetic regulation of paired antagonistic NLRs, providing a tool to develop elite crop varieties.
Crop diseases threaten global food security and sustainable agriculture. The most efficient strategy to prevent disease is to develop crop varieties with durable and broad-spectrum resistance (1, 2). Rice blast, caused by the fungal pathogen Magnaporthe oryzae (Pyricularia oryzae) (3), is the most devastating rice disease.
The indigenous Chinese rice variety Gumei 4 (GM4) has been used as a blast resistance donor in breeding for over 50 years. GM4-derived varieties or nearisogenic lines (NIL-Pigm) with the Pigm resistance locus (4) display high and durable blast resistance without change in resistance to other pathogens (Fig. 1A and fig. S1), with a spectrum broader than other known Pi genes such as Pi9/Pi2/Pizt (5, 6) (Fig. 1B and table S1). Moreover, the Pigm locus has been used in breeding nationwide (table S2).
However, the molecular mechanism of Pigm underlying disease resistance was unclear. We further mapped Pigm to an interval within a BAC contig from GM4 based on our previous study (4) (Fig. 1C). We sequenced the BAC contig covering Pigm and uncovered a cluster of 13 NLR genes including three intact transcribed NLRs (R4, R6 and R8) (fig. S2), ten potential pseudogenes (R1, R2, R3, R5, R7, R9-R13), and one Ty3/gypsy retrotransposon (Fig. 1D). The genomic sequence of the Pigm locus displayed similarity to the Pi2, Pi9 and wild rice clusters in the same region (fig. S3, A and B), suggesting that Pigm locus might be selected during domestication from an ancient locus.
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