DNA hypomethylation in tetraploid rice potentiates stress-responsive gene expression for salt tolerance

Abstract

Polyploidy is a prominent feature for genome evolution in many animals and all flowering plants. Plant polyploids often show enhanced fitness in diverse and extreme environments, but the molecular basis for this remains elusive. Soil salinity presents challenges for many plants including agricultural crops. Here we report that salt tolerance is enhanced in tetraploid rice through lower sodium uptake and correlates with epigenetic regulation of jasmonic acid (JA)–related genes. Polyploidy induces DNA hypomethylation and potentiates genomic loci coexistent with many stress-responsive genes, which are generally associated with proximal transposable elements (TEs). Under salt stress, the stress-responsive genes including those in the JA pathway are more rapidly induced and expressed at higher levels in tetraploid than in diploid rice, which is concurrent with increased jasmonoyl isoleucine (JA-Ile) content and JA signaling to confer stress tolerance. After stress, elevated expression of stress-responsive genes in tetraploid rice can induce hypermethylation and suppression of the TEs adjacent to stress-responsive genes. These induced responses are reproducible in a recurring round of salt stress and shared between two japonica tetraploid rice lines. The data collectively suggest a feedback relationship between polyploidy-induced hypomethylation in rapid and strong stress response and stress-induced hypermethylation to repress proximal TEs and/or TE-associated stress-responsive genes. This feedback regulation may provide a molecular basis for selection to enhance adaptation of polyploid plants and crops during evolution and domestication.

A Genome Doubling Event Reshapes Rice Morphology and Products by Modulating Chromatin Signatures and Gene Expression Profiling

“…Partial pollen and embryo sac sterilities are the two important factors that lead to low seed set in autotetraploid rice (Li et al 2017;Wu et al 2014). Because excellent salt tolerance is enhanced in tetraploid rice (Wang et al 2021), we also noticed that the genes related to physiological and ecological tolerance were changed in autotetraploids, which might be related to the environmentally adaptive phenotypes of autotetraploids (Additional file 6: Table S5).…”

“…Similarly, autotetraploid rice from another indica diploid cultivar displayed similar phenotypes at mature stages, including increased leaf sizes, decreased fertility, fewer branches, reduced spikelet numbers, and enlarged grain sizes (Zhang et al 2015). Moreover, despite strong biomass production and higher resistance against abiotic and biotic stresses (Wu et al 2013;Wang et al 2021), autotetraploid rice has poor seed set, which has become the largest bottleneck and the major barrier in commercial production (Wu et al 2014;Guo et al 2017). Partial pollen and embryo sac sterilities are the two important factors that lead to low seed set in autotetraploid rice (Li et al 2017;Wu et al 2014).…”

“…These findings suggest that the irregular TEs associated with the hypo-methylation and downregulation of 24-nt TE-siRNAs result in an autotetraploid rice incompatibility response to "genomic shock" by polyploidization and probably disturb chromatin structure during autotetraploid rice meiosis. In addition, salt tolerance is enhanced in tetraploid rice through lower sodium uptake and correlates with DNA methylation controlling jasmonic acid-related genes (Wang et al 2021). In addition to DNA methylation, genome duplication contributes to the switching of some loose and compact structural domains with an altered histone modification status, including H3K4me3 and H3K27me3 in the Arabidopsis genome, which modulates genome-wide transcription (Zhang et al 2019).…”

“…To better understand how natural selection enables neopolyploidy to overcome early challenges is an urgent issue for biologists. Given that allopolyploids can be confounded by the entanglement of both WGD and hybridization, synthesized autopolyploid systems are ideal systems to investigate the short-term effects produced by WGDs, such as those in Arabidopsis (Zhang et al 2019), rice (Chen et al 2019;Wu et al 2017;Yu et al 2020;Guo et al 2017;Wang et al 2021), potato (Stupar et al 2007), Citrus limonia (Allario et al 2011) and willows (Dudits et al 2016). To some extent, according to these results, it is possible that the change in transcriptional activity induced by autotetraploid plants could be attributed to nuclear dosage (Riddle et al 2010;Stupar et al 2007;Allario et al 2011).…”

Designed breeding for adaptation of crops to environmental abiotic stresses

“…。在干旱期间，植物通过增加根系的吸水能力、关闭气孔 减少水分的流失、调节组织内的渗透势等来维持生理水分的平衡 [4] 。在细胞水平上，干 旱信号促进了脯氨酸和海藻糖等应激保护代谢物的产生，触发抗氧化系统以维持氧化还 A c c e p t e d https://engine.scichina.com/doi/10.1360/SSV-2021-0162 原反应的稳态，防止急性细胞损伤和维持膜的完整性。除此之外，也会触发特定的信号 响应，比如脱落酸(abscisic acid, ABA) 、油菜素内酯(brassinosteroids, BR) 、乙烯 (ethylene)等植物激素途径 [5] 。比如干旱胁迫促进脱落酸的积累，通过激酶活性调节作 用靶向包括离子通道和转录因子在内的底物蛋白，将信号进行级联传递来应答干旱胁迫 [6] 。 植物能够通过调控根部形态和蒸腾效率提高抗旱性，比如水稻中的编码生长素应答 DRO1 [7] 、拟南芥和水稻的类受体蛋白激酶 ERECTA(ER) [8] ，以及水稻、小麦、玉米 中具有抗旱调控作用的转录因子家族，包括 DREB、ERF、WRKY、ZFP、MYB 基因家 族成员等。 目前陆续从不同作物中克隆到大量关于提高植物抗旱性的基因， 如 OsNAC5、 OsNAC9、OsNAC10 在水稻中过量表达显著提高抗旱能力，有助于增加水稻在干旱胁迫 下的总产量 [4] ；此外 OsbZIP 家族成员也发挥着关键作用，如以 OsbZIP46 为核心的干旱 应答精细调控网络，同样能够赋予水稻更强的耐旱性 [9] ；以及 ERF 家族的成员 OsERF4a 和 DREB 的成员 OsDREB2B，超表达株系均能够增强水稻在干旱胁迫环境中的耐受能 力 [10] ，这些调控因子的深度挖掘为水稻抗旱遗传改良提供新思路。小麦是重要的粮食资 源，超量表达 TaERF1、TaERF3 均能提高小麦对干旱胁迫的耐受性；TaZFP34 通过改变 根的形态建成，增强根伸长的能力，提高小麦抗旱性 [11] 。研究发现小麦中类受体蛋白激 酶 TaER1 和 TaER2 正调控叶片大小，进而会增强水分利用效率、提高生物量积累和单 株产量 [11] 。除此之外，研究发现三种胞质甘油醛-3-磷酸脱氢酶(TaGAPC2/5/6)通过活 性氧清除和气孔运动，正向调控小麦对干旱胁迫的响应 [12] 。水分是维持植物生长发育所 必需的，玉米在开花过程需要充足的水分以确保正常的受精和结实，干旱胁迫会导致玉 米单产持续下降。研究表明 NAC 基因 ZmNAC111 启动子中的转座子插入影响玉米对干 旱敏感性 [13] 。此外，玉米中 NAC 转录因子 NUT1 参与调控次级细胞壁的生物合成和分 解，控制木质部细胞壁厚度和强度，从而影响玉米的干旱和高温响应 [14] [22][23][24][25][26][27][28][29][30][31][32] 。最近的一项研究发现，SOS2 同家族蛋白 CIPK8 的功能与 SOS2 的功能类似，介 导拟南芥的盐稳态 [33] 。 除了 SOS3/SCaBP8 外， GRIK (Geminivirus Rep Interaction Kinase) 1 和 GRIK2 蛋白也可以磷酸化并激活 SOS2 的活性，以提高植物的耐盐性 [34] 。PA 激活 的 MPK6 可以磷酸化和激活 SOS1 [35] 。盐胁迫缓解后，BIN2 磷酸化并抑制 SOS2，从而 平衡胁迫响应和植物生长 [36] 。正常条件下，蛋白激酶 PKS5 磷酸化 SOS2，GI 及 14-3-3 [37][38][39][40] [45] 。参与表观修饰作用的 AGO 蛋白也参与调控水稻耐盐性。近 期研究发现，过表达水稻 AGO2 可增加谷粒大小和耐盐性，通过直接调控嘌呤转运活性 的通透酶 BG3 启动子区 H3K4me3 和 H3K27me3 修饰水平促进其表达， 控制细胞分裂素 的分布模式，进而影响水稻响应逆境和谷粒的发育…”