A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy

A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy
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DOI:
10.1111/tpj.13136
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发表时间:
2016-03-01
期刊:
影响因子:
7.2
通讯作者:
Gallois, Jean-Luc
Gallois, Jean-Luc
中科院分区:
生物学1区
文献类型:
--
作者:
Gauffier, Camille;Lebaron, Caroline;Gallois, Jean-Luc

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对病原体的遗传抗性对于可持续地维持作物产量是重要的。最近的生物技术提供了通过补偿自然抗性缺失来产生抗性植物的替代方法。番茄(Solanum lycopersicum)及其近缘种提供了一个模型,可以比较天然和耕作诱导的多病毒抗性等位基因。对于基于翻译起始因子eIF4E1的抗性,我们证实了从野生番茄Solanum habrochaites中分离的天然等位基因Sh-eIF4E1(PI24)-pot1与对马铃薯Y病毒和烟草etch病毒分离物的广泛抗性有关。相比之下,通过TILLING策略从栽培番茄S.lycopersicum中分离出的同一基因的空等位基因与更窄的抗性谱相关。将该空等位基因渗入单倍体并没有扩大单倍体的抗性谱,说明遗传背景不是单倍体广泛抗性的原因。相反,不同类型的eIF4E1突变对eIF4E2水平的影响不同,这表明eIF4E2也参与了对多病毒的抗性。事实上,结合影响eIF4E1和eIF4E2的两个零突变,在栽培番茄中重新建立了广泛的抗性谱,但不利于植株发育。这些结果突出了eIF4E基因家族中的冗余效应,其中表达调控改变了对多病毒的易感性或抗性。在作物改良方面,使用功能丧失等位基因产生抗性可能会适得其反,如果它们缩小了抗性谱并限制了生长。使用与自然多样性中发现的功能变异相似的等位基因编码可能更有效。新的抗性性状是植物育种的重要目标。在这里,我们比较了野生番茄中一个功能性的天然eIF4E等位基因与栽培番茄中tillin产生的零等位基因的差异,该等位基因广泛赋予了对马铃薯Y病毒和烟草蚀刻病毒的抗性。由于TILLING等位基因的冗余性,除非将两个基因的零突变组合在一起,否则TILLING等位基因的有效性不高,并且双突变体损害了植物的生长。这些结果表明,无效等位基因不一定适合在作物中产生广谱抗性。
Genetic resistance to pathogens is important for sustainable maintenance of crop yields. Recent biotechnologies offer alternative approaches to generate resistant plants by compensating for the lack of natural resistance. Tomato (Solanum lycopersicum) and related species offer a model in which natural and TILLING-induced potyvirus resistance alleles may be compared. For resistance based on translation initiation factor eIF4E1, we confirm that the natural allele Sh-eIF4E1(PI24)-pot1, isolated from the wild tomato species Solanum habrochaites, is associated with a wide spectrum of resistance to both potato virus Y and tobacco etch virus isolates. In contrast, a null allele of the same gene, isolated through a TILLING strategy in cultivated tomato S.lycopersicum, is associated with a much narrower resistance spectrum. Introgressing the null allele into S.habrochaites did not extend its resistance spectrum, indicating that the genetic background is not responsible for the broad resistance. Instead, the different types of eIF4E1 mutations affect the levels of eIF4E2 differently, suggesting that eIF4E2 is also involved in potyvirus resistance. Indeed, combining two null mutations affecting eIF4E1 and eIF4E2 re-establishes a wide resistance spectrum in cultivated tomato, but to the detriment of plant development. These results highlight redundancy effects within the eIF4E gene family, where regulation of expression alters susceptibility or resistance to potyviruses. For crop improvement, using loss-of-function alleles to generate resistance may be counter-productive if they narrow the resistance spectrum and limit growth. It may be more effective to use alleles encoding functional variants similar to those found in natural diversity.Significance Statement New resistance traits are important targets for plant breeding. Here we compared a functional natural eIF4E allele in a wild tomato species, which broadly conferred resistance to Potato virus Y and Tobacco etch virus, to TILLING-generated null alleles in cultivated tomato. Due to gene redundancy, the TILLING alleles were not as effective unless null mutations in two genes were combined, and the double mutant had impaired plant growth. These results indicate that null alleles are not necessarily suitable for generating broad spectrum resistance in crops.