Competitive trans-generational control of seed dormancy via stable inheritance of gametophytic epigenomes

在繁殖过程中，进化理论表明，为了使后代的适应性最大化，父母可能会有相互冲突的最佳策略。出现这种情况的一个例子是，当雄性产生一小部分雌性后代时：在这种情况下，母性的最佳策略是将资源分配给后代，并尽量减少亲属之间的竞争，而父亲则通过允许后代隔离资源并与亲属竞争而获得优势。在植物中，即使是在以自交为主的物种中，也有明显的亲代冲突的例子，例如在调节种子大小方面。增加拟南芥种子母本基因组剂量导致种子变小，而增加父本基因组剂量导致种子变大。这些冲突不是在胚胎中发生的，而是在第二种种子组织——胚乳中发生的。开花植物与其他植物谱系的区别在于双受精过程：每个花粉粒中的两个精子细胞使卵细胞受精产生胚胎，但也使胚珠的中心细胞受精产生胚乳。胚乳在种子大小的控制中起着关键作用，父母亲对种子大小的相互冲突影响通过在配子中建立并遗传到胚乳中的不同表观基因组来发挥作用。这些表观基因组导致所谓的“印记”基因表达，即只从一个亲本遗传的等位基因在胚乳发育期间表达。例如，如果父亲的等位基因以表观遗传的“开”状态遗传，那么父亲表达的印迹基因就会出现，而母亲的等位基因则以表观遗传的“关”状态遗传。胚乳保留在大多数物种的成熟种子中，在种子休眠和萌发中起关键作用，之后经历程序性细胞死亡。萌发终止了种子的传播，从而在空间和时间上对后代的分布起着作用。一个关于植物繁殖过程中亲代冲突的数学理论的进一步预测是，母亲应该倾向于增加休眠，以分散后代和减少竞争，而父亲应该倾向于快速发芽，以战胜后代，并确保离母亲更近的有利生态位。在控制种子休眠过程中是否真的发生亲代冲突仍然是一个悬而未决的问题，但最近有研究表明，印迹基因在胚乳中控制种子休眠中发挥了作用。最近，我们已经证明，即使在种子传播之后，母体表观基因组仍稳定地保留在胚乳中，并且对种子休眠的发育和胚胎行为的控制至关重要，并从母体基因组中确定了施加种子休眠的特定染色质重塑复合物。在这里，我们还表明，增加父本基因组剂量在胚乳导致相同的低休眠表型。这提出了一个新的假设，即亲本表观基因组在胚乳中竞争，以控制后代种子的休眠和萌发行为。本研究详细描述了亲本表观基因组在调节种子休眠的胚乳中的作用，并旨在通过对关键发育阶段的印迹基因的研究，确定父亲表观遗传状态促进低休眠的靶基因和过程。由于种子凝固过程中环境温度的变化促进了种子的休眠，因此需要了解温度如何以及温度是否通过相同的染色质重塑过程影响种子的休眠和萌发。

During reproduction evolutionary theory has shown that parents can have conflicting optimal strategies for maximising fitness of their offspring. One example where this situation arises is when males give rise to a fraction of the female brood: in this case the optimal maternal strategy is to distribute resources among progeny and minimise competition between kin, while fathers gain an advantage by allowing progeny to sequester resources and outcompete kin. In plants, even in predominantly selfing species, there are clear examples of parental conflict such as in the regulation of seed size. Increasing the maternal genome dose in Arabidopsis seeds leads to smaller seeds, whereas increasing the paternal genome dose leads to larger seeds. These conflicts do not play out in the embryo but in a second seed tissue called the endosperm. Flowering plants are distinguished from other plant lineages by the process of double fertilisation: two sperm cells in each pollen grain fertilise the egg cell to create the embryo, but also the central cell of the ovule to create the endosperm. The endosperm plays a key role in the control of seed size, and the conflicting influences of the mother and father on seed size are played out through distinctive epigenomes which are established in the gametes and inherited into the endosperm. These epigenomes lead to so-called 'imprinted' gene expression where the allele inherited from only one parent is expressed during endosperm development. For instance paternally expressed imprinted genes arise if the paternal allele is inherited in an epigenetic 'on' state, whereas the maternal alleles are inherited in an epigenetic 'off' state. The endosperm is retained in mature seeds of most species and plays a key role in seed dormancy and germination, after which it undergoes programmed cell death. Germination terminates seed dispersal and so plays a role in distributing progeny in space and time. One further prediction of mathematical theories of parental conflict during plant reproduction is that mothers should favour increased dormancy to disperse progeny and reduce competition, whereas fathers should favour fast germination to outcompete progeny and secure favourable niches closer to the mother plant. It remains an open question whether parental conflicts really occur in the control of seed dormancy but recently it has been shown that imprinted genes can play a role in seed dormancy control in the endosperm.Recently we have shown that the maternal epigenome is retained stably in the endosperm even after seed dispersal and is essential for the development of seed dormancy and the control of embryo behaviour, and identified specific chromatin remodelling complexes that impose seed dormancy from the maternal genome. Here we also show that increasing the paternal genome dose in the endosperm leads to an identical low dormancy phenotype. This raises the novel hypothesis that parental epigenomes compete in the endosperm to control progeny seed dormancy and germination behaviour. This proposal describes a detailed characterisation of the roles of parental epigenomes in the endosperm that regulate seed dormancy and aims to identify the target genes and processes by which the father's epigenetic state promotes low dormancy, via the study of imprinted genes at the critical developmental stages. Because seed dormancy is promoted by changes in environmental temperature during seed set, this requires understanding how temperature and whether temperature acts through the same chromatin remodelling processes to affect seed dormancy and germination.