2022, Vol. 38中国科学院微生物研究所、中国微生物学会主办
文章信息
- 刘子茜, 朱雅欣, 伍国强, 魏明
- LIU Zixi, ZHU Yaxin, WU Guoqiang, WEI Ming
- SnRK2在植物响应逆境胁迫和生长发育中的作用
- The role of SnRK2 in the response to stress, the growth and development of plants
- 生物工程学报, 2022, 38(1): 89-103
- Chinese Journal of Biotechnology, 2022, 38(1): 89-103
- 10.13345/j.cjb.210267
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文章历史
- Received: March 30, 2021
- Accepted: July 7, 2021
引用本文
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干旱、高盐、极端温度等是制约植物生长发育和作物产量的主要环境因素。为了应对这些不利环境，植物在长期的进化中逐渐形成了一系列的生理和分子适应机制。其中，蛋白磷酸化和去磷酸化在植物响应逆境胁迫信号转导中发挥重要作用[1]。蛋白磷酸化是一个可逆的过程，由蛋白激酶和蛋白磷酸酶两种拮抗酶催化。蛋白激酶通过感知各种环境信号，激活不同蛋白磷酸化途径调控下游靶标基因的表达，以保护植物免受各种逆境胁迫的伤害[2]。植物蛋白激酶主要有受体蛋白激酶(receptor-like protein kinases, RLK)、丝裂原活化蛋白激酶(mitogen-activated protein kinase, MAPK)、钙依赖蛋白激酶(calmodulin-dependent protein kinases, CDPK) 以及蔗糖非发酵-1-相关蛋白激酶(sucrose non-fermenting-1-related protein kinase, SnRK) 等。
SnRK是一类Ser/Thr蛋白激酶，具有高度的保守性。根据序列相似性、结构及功能不同，可将其分为3个亚家族：SnRK1、SnRK2和SnRK3。SnRK1在结构和功能上与酵母蔗糖非发酵1 (sucrose non-fermenting 1, SNF1) 和哺乳动物AMPK (AMP-activated protein kinase) 具有较高的相似性，在代谢调节过程中发挥重要作用[3]。SnRK2参与渗透胁迫及脱落酸(abscisic acid, ABA) 应答，在胁迫信号转导中起重要作用[4]。SnRK3通过与钙调磷酸酶B蛋白(calcineurin B-like proteins, CBL) 结合，又被称作CBL相互作用蛋白激酶(CBL-interacting protein kinases, CIPK)，参与各种生物和非生物的逆境胁迫反应，并调节植物的生长和发育。
SnRK2在生物和非生物逆境胁迫应答中发挥多重功能，已有大量文献对不同物种SnRK2的功能进行了探究，但对该蛋白激酶的生物学功能及其调控机制尚未完全解析。为促进SnRK2家族在作物遗传改良的功能探索和应用，结合笔者所在研究团队对甜菜(Beta vulgaris L.) BvSnRK2家族的研究成果，本文系统总结了植物SnRK2的发现、分类及结构，重点对SnRK2响应各种逆境胁迫和调控生长发育的研究成果加以综述，并对其未来的研究方向进行了展望。
1 SnRK2的发现SnRK2是一个相对较小的蛋白激酶亚家族。最早发现的SnRK2成员是从小麦(Triticum aestivum L.) 中克隆到的PKABA1 (ABA-induced protein kinase)，该基因受ABA和干旱胁迫的诱导[5]。随后，在许多植物中鉴定到SnRK2成员(表 1)。笔者采用生物信息学手段，从基因组水平上鉴定出6个甜菜SnRK2，将其命名为BvSnRK2.1–BvSnRK2.6 [6]。在水稻(Oryza sativa L.)、甜樱桃(Prunus avium L.) 和大豆(Glycine max L.) 中分别发现10、6和22个成员[7-9]，水稻由于其家族成员均被高渗透胁迫诱导，因此又称之为SAPKs (stress-activated protein kinases)[7]。这些结果表明，不同物种间SnRK2s数量存在显著差异。这种数量上的差异可能与其进化过程中基因的重复、缺失及基因组多倍体有关，一般来说，二倍体物种中的数量少于四倍体、六倍体和八倍体[10]。
| Species | Gene number | Gene member | Ploidy | Class | References |
| Arabidopsis thaliana L. | 10 | AtSnRK2.1–AtSnRK2.10 | 2 | Dicotyledon | [11] |
| Zea mays L. | 11 | ZmSnRK2.1–ZmSnRK2.11 | 2 | Monocotyledon | [12] |
| Sorghum bicolor L. | 10 | SbSnRK2.1–SbSnRK2.10 | 2 | Monocotyledon | [13] |
| Oryza sativa L. | 10 | OsSAPK1–OsSAPK10 | 2 | Monocotyledon | [7] |
| Malus prunifolia Borkh. | 12 | MpSnRK2.1–MpSnRK2.12 | 2 | Dicotyledon | [14] |
| Brachypodium distachyon L. | 10 | BdSnRK2.1–BdSnRK2.10 | 2 | Monocotyledon | [15] |
| Vitis vinifera L. | 8 | VviSnRK2.1–VviSnRK2.8 | 2 | Dicotyledon | [16] |
| Brassica napus L. | 10 | BnSnRK2.1–BnSnRK2.10 | 4 | Dicotyledon | [17] |
| Triticum aestivum L. | 10 | TaSnRK2.1–TaSnRK2.10 | 6 | Monocotyledon | [18] |
| Gossypium hirsutum L. | 20 | GhSnRK2.1–GhSnRK2.20 | 4 | Dicotyledon | [19] |
| Hevea brasiliensis Muell. Arg. | 10 | HbSnRK2.1–HbSnRK2.10 | 3 | Dicotyledon | [20] |
| Prunus avium L. | 6 | PacSnRK2.1–PacSnRK2.6 | 2 | Dicotyledon | [8] |
| Glycine max L. | 22 | GmSnRK2.1–GmSnRK2.22 | 4 | Dicotyledon | [9] |
| Populus trichocarpa Torr. & Gray. | 12 | PtSnRK2.1–PtSnRK2.12 | 2 | Dicotyledon | [21] |
| Musa acuminate L. | 11 | MaSnRK2.1–MaSnRK2.11 | 3 | Monocotyledon | [22] |
| Saccharum officinarum L. | 10 | SoSnRK2.1–SoSnRK2.10 | 4 | Monocotyledon | [23] |
| Camellia sinensis L. | 8 | CsSnRK2.1–CsSnRK2.8 | 2 | Dicotyledon | [24] |
| Setaria viridis L. | 11 | SvSnRK2.1–SvSnRK2.11 | 2 | Monocotyledon | [25] |
| Eucalyptus grandis H. | 8 | EgrSnRK2.1–EgrSnRK2.8 | 4 | Dicotyledon | [26] |
| Pyrus bretschneideri Rehd. | 10 | PbrSnRK2.1–PbrSnRK2.10 | 2 | Dicotyledon | [27] |
| Beta vulgaris L. | 6 | BvSnRK2.1–BvSnRK2.6 | 2 | Dicotyledon | [6] |
| Fragaria vesca L. | 9 | FvSnRK2.1–FvSnRK2.9 | 2 | Dicotyledon | [28] |
| Capsicum annuum L. | 9 | CaSnRK2.1–CaSnRK2.9 | 2 | Dicotyledon | [29] |
SnRK2是一类相对较小的蛋白激酶亚家族，分子量(MWs) 大约为40 kDa。所有SnRK2的氨基酸序列可分为2个区域，一个是与SNF1和AMPK相关的高度保守的N端激酶结构域，另一个是差异明显的C端调节结构域。C端调节结构域在功能上又进一步分为结构域Ⅰ和结构域Ⅱ。结构域Ⅰ是由靠近N端激酶结构域的约30个氨基酸组成，存在于所有SnRK2成员中，主要受逆境胁迫诱导; 结构域Ⅱ大约含有40个氨基酸，仅在结构域Ⅰ之后，是响应ABA应答的必需元件，属于ABA依赖型SnRK2成员所特有的[30]。根据C端氨基酸的酸性不同，SnRK2可分为富含天冬氨酸(Asp) 的SnRK2a和富含谷氨酸(Glu) 的SnRK2b;又可根据是否受ABA诱导，将其分为第Ⅰ、Ⅱ、Ⅲ组，其中第Ⅰ组成员不受ABA诱导，第Ⅱ组受ABA弱诱导，而第Ⅲ组受ABA强烈诱导。结构域Ⅰ在所有的SnRK2家族成员中存在，而结构域Ⅱ仅存在于第Ⅲ组成员中。笔者对甜菜BvSnRK2s家族成员分析发现，MWs从37.8 kDa到41.15 kDa不等，蛋白序列长度为335–364个氨基酸; N端序列高度保守，C端则差异很大。N端有两个保守的结构域，ATP结合位点(D/Q/NI/LGS/AGNFGVA)和蛋白激酶激活位点(CHRDLKLENTLLD)，是BvSnRK2激活所必需的[6]。这与SnRK2所特有的结构特点相一致。以拟南芥AtSnRK2序列为查询序列，通过NCBI数据库搜索单子叶(小麦、玉米) 和双子叶植物(陆地棉、甜菜、苹果) SnRK2s的蛋白序列，根据Ser/Thr蛋白激酶结构域，剔除冗余序列和不完全序列，共鉴定出59条非冗余SnRK2序列。在此基础上，利用MEGA X软件构建SnRK2的系统发育树(图 1)。结果表明，59个SnRK2蛋白可分为3大类，第Ⅰ、Ⅱ、Ⅲ组分别含有19、19、21个成员。另外，双子叶植物陆地棉、苹果SnRK2成员数量比单子叶植物小麦和玉米多。此外，处于同一分支的成员具有更高的同源性、基本结构和功能相似性。甜菜BvSnRK2.2和BvSnRK2.3属于第Ⅰ组; BvSnRK2.1和BvSnRK2.4属于第Ⅱ组; BvSnRK2.5和BvSnRK2.6则属于第Ⅲ组。结构域Ⅰ在所有6个成员中均存在，结构域Ⅱ仅在BvSnRK2.5和BvSnRK2.6中发现[6]。在小麦的10个SnRK2s成员中，TaSnRK2.3、TaSnRK2.4、TaSnRK2.6、TaSnRK2.7和TaSnRK2.8属于第Ⅰ组; TaSnRK2.1、TaSnRK2.2和TaSnRK2.5属于第Ⅱ组; TaSnRK2.9和TaSnRK2.10属于第Ⅲ组[18]。在ABA处理下，第Ⅲ组TaSnRK2s被强烈诱导，第Ⅱ组被弱诱导，第Ⅰ组则不被ABA处理激活; 而在渗透胁迫下所有TaSnRK2s均被激活[18]。另外，山茶树中共发现8个SnRK2基因，ABA强烈诱导第Ⅲ组成员CsSnRK2.5、CsSnRK2.6和CsSnRK2.7，弱诱导CsSnRK2.1和CsSnRK2.8，而CsSnRK2.3被ABA显著抑制[24]。Duarte等分析了狗尾草(Setaria viridis L.) 中11个SnRK2家族基因，在干旱和盐胁迫下，第Ⅰ组SvSnRK2.10和SvSnRK2.11及第Ⅱ组SvSnRK2.4和SvSnRK2.9最为敏感，而第Ⅲ组SvSnRK2s成员被ABA强烈激活，作为ABA信号正向调节因子[25]。这些结果表明，渗透胁迫均可诱导所有SnRK2成员，而ABA仅强烈诱导第Ⅲ组成员。渗透胁迫和ABA对SnRK2的激活可通过不同蛋白的磷酸化来介导，但以SnRK2为蛋白的下游靶标基因报道相对较少，未来需要进一步研究。
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| 图 1 高等植物SnRK2s系统进化树 Fig. 1 Phylogenetic tree of the higher plant SnRK2s. Clustal W software was used for multiple alignment of sequences, the phylogenetic tree was constructed using MEGA X software. The source, name and registration number of SnRK2 protein are as follows: Gossypium hirsutum GhSnRK2.1 (Gh_A01G0057), GhSnRK2.2 (Gh_A02G0789), GhSnRK2.3 (Gh_A03G1684), GhSnRK2.4 (Gh_A05G1922), GhSnRK2.5 (Gh_A10G1380), GhSnRK2.6 (Gh_A11G0474), GhSnRK2.7 (Gh_A11G1757), GhSnRK2.8 (Gh_A11G1858), GhSnRK2.9 (Gh_A11G3023), GhSnRK2.10 (Gh_A12G0641), GhSnRK2.11 (Gh_D01G0057), GhSnRK2.12 (Gh_D02G0839), GhSnRK2.13 (Gh_D02G2104), GhSnRK2.14 (Gh_D05G2155), GhSnRK2.15 (Gh_D10G1083), GhSnRK2.16 (Gh_D11G0489), GhSnRK2.17 (Gh_D11G0552), GhSnRK2.18 (Gh_D11G2149), GhSnRK2.19 (Gh_D11G3472) and GhSnRK2.20 (Gh_D12G0859); Beta vulgaris BvSnRK2.1 (Bv1_008630_pooe), BvSnRK2.2 (Bv4_084120_kqpu), BvSnRK2.3 (Bv5_105400_zmyx), BvSnRK2.4 (Bv6_138530_ywks), BvSnRK2.5 (Bv6_134600_gdoe) and BvSnRK2.6 (Bv9_218570_fxdy); Triticum aestivum TaSnRK2.1 (ALL27272.1), TaSnRK2.2 (AIK01699.1), TaSnRK2.3 (ALL27273.1), TaSnRK2.4 (ACU65228.1), TaSnRK2.5 (ABD37622.1), TaSnRK2.6 (QDA34126.1), TaSnRK2.7 (ALL27274.1), TaSnRK2.8 (ACU65228.1), TaSnRK2.9 (QBH75449.1) and TaSnRK2.10 (AIY30425.1); Zea mays ZmSnRK2.1 (ACG50005.1), ZmSnRK2.2 (ACG50006.1), ZmSnRK2.3 (ACG50007.1), ZmSnRK2.4 (ACG50008.1), ZmSnRK2.5 (ACG50009.1), ZmSnRK2.6 (ACG50010.1), ZmSnRK2.7 (ACG50011.1), ZmSnRK2.8 (ACG50012.1), ZmSnRK2.9 (NP_001130186.1), ZmSnRK2.10 (ACG50013.1) and ZmSnRK2.11 (ACG50014.1); Malus prunifolia MpSnRK2.1 (AIK22403.1), MpSnRK2.2 (AIK22405.1), MpSnRK2.3 (AIK22409.1), MpSnRK2.4 (AIK22404.1), MpSnRK2.5 (AIK22399.1), MpSnRK2.6 (AIK22408.1), MpSnRK2.7 (AIK22406.1), MpSnRK2.8 (AIK22402.1), MpSnRK2.9 (AIK22400.1), MpSnRK2.10 (AIK22401.1), MpSnRK2.11 (AIK22398.1) and MpSnRK2.12 (AIK22407.1). |
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SnRK2在植物响应非生物胁迫中发挥着信号转导作用，并被渗透胁迫所激活。磷酸化对于激活SnRK2有促进作用，激酶激活环的可逆磷酸化是调节SnRK2活性的原因[31]。烟草(Nicotiana tabacum L.) 渗透应激活化蛋白激酶(osmotic stress-activated protein kinase, NtOSAK) 是SnRK2亚家族成员之一，在高渗透胁迫应答中被迅速激活[32]。Burza等通过在玉米原生质体中瞬时表达NtOSAK并进行突变，证实Ser154和Ser158磷酸化位点参与调控NtOSAK活性。进一步的研究发现，Ala或Glu替代Ser154或Ser158后，激酶活性消失，说明酸性氨基酸残基不能替代NtOSAK磷酸化的Ser154或Ser158，这两个氨基酸残基在NtOSAK激活中起重要作用[33]。Boudsocq等采用一种磷酸蛋白专用染料(pro-Q diamond) 证明，所有被激活的SnRK2都在渗透胁迫下发生了磷酸化反应。此外，ABA诱导的磷酸化水平明显低于渗透胁迫[34]，表明渗透胁迫和ABA激活SnRK2的机制有所不同。目前已鉴定的多个SnRK2磷酸化位点，其中体外激酶检测发现ZmSAPK8优先选择Mn2+和Mg2+作为磷酸化的辅助因子，激活环中的Ser182和Thr183可能分别是上游激活和抑制磷酸化的重要靶点[35]。另外，Ser175的突变极大地影响了激酶磷酸化底物的能力，表明Ser175对“SnRK2特异性结构域”的生化活性至关重要，该机制是SnRK2家族激酶所共有的[36]。类似的磷酸化位点在AtSnRK2.10的Ser158也被发现，并参与调节渗透胁迫反应[37]。这些结果表明，激酶激活环中的可逆磷酸化参与SnRK2在应对环境胁迫时的激活，磷酸化对激酶活性至关重要。
3.2 SnRK2与ABA相互作用ABA是植物在干旱和高盐等渗透胁迫下积累的一种关键的胁迫信号激素，能够协调生理和代谢反应，以使植物适应逆境[38]。SnRK2参与ABA信号转导从而实现对非生物胁迫的应答。在ABA依赖信号通路中，第Ⅲ组SnRK2成员是信号转导的枢纽，组成ABA-PYR (pyrabactin resistance)-PP2C (protein phosphatases 2C)-SnRK2偶联的信号通路，从而启动磷酸化转录因子和离子通道[39]。在ABA缺失情况下，PP2C通过物理相互作用抵消SnRK2，此时SnRK2没有活性，从而抑制介导ABA应答基因表达的转录因子激活。在ABA存在情况下，PP2C与ABA受体RCAR (regulatory components of ABA receptor)/ PYR/PYL (PYR-like) 结合后，RCAR/PYR/ PYL-PP2C复合物的构象发生变化，使其与PP2C互作，并激活SnRK2，从而磷酸化下游底物以介导应激反应[40]。可见，PP2C在ABA信号转导中起着交换机制的作用。另外，Raf类蛋白激酶(Raf-like protein kinases, RAFs) 参与ABA引发的SnRK2激活。SnRK2通过PP2C释放后被RAFs快速激活，并且激活的SnRK2可对更多未被激活的SnRK2s进行磷酸化。可见，在ABA核心信号通路中，RAF-SnRK2级联反应可以激活并扩大胁迫信号(图 2)[41]。在ABA非依赖信号通路中，SnRK2不被ABA激活，而在ABA积累之前就被渗透胁迫直接激活[31]。3种B4型Raf类蛋白激酶(mitogen-activated protein kinase kinase kinases, MAPKKKs) 可在渗透胁迫下磷酸化并激活第Ⅰ组SnRK2成员(图 2)，表明MAPKKKs是ABA非依赖的第Ⅰ组成员的上游因子，可直接被渗透胁迫激活[42]。磷脂酸(phosphatidic acid, PA) 参与调节植物生长发育，与ABA非依赖的SnRK2互作，实现SnRK2信号通路在不同水平上的调控，完成植物复杂的信号转导[43]。特异性Ca2+结合蛋白(SnRK2-interacting calcium sensor, SCS) 在种子萌发过程中参与对ABA的响应，与SnRK2相互作用，并抑制SnRK2活性(图 2)[44]。另外，ABA诱导的NO使得SnRK2失活，负向调控ABA信号转导途径[45]。
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| 图 2 SnRK2是多功能调控因子 Fig. 2 SnRK2 is a multi-functional regulator. ABA (abscisic acid); PYR/PYL/RCAR (ABA receptor); PP2C (protein phosphatases 2C); ABI1/ABI5 (ABA-insensitive); HOS15 (high expression of osmotically responsive 15); RAF (raf-like protein kinases); TFs (transcription factors); SLAC1 (slow anion channel 1); KAT1 (inward-rectifying potassium channel); NADPH (oxidase); NO (nitric oxide); PA (phosphatidic acid); SCS (SnRK2-interacting calcium sensor); MAPKKK (mitogen-activated protein kinase kinase kinases); P (phosphorylation). |
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植物生长在不断变化的环境中，必须对环境作出迅速感知，需要对ABA信号进行动态调控。尽管SnRK2是ABA信号通路的主要调控者，但对于其在ABA信号终止后的反馈调控却知之甚少。最新研究发现，ABA信号终止子(ABA signaling terminator, ABT) 通过阻断PYR1-ABI1 (ABA-insensitive1) 相互作用来关闭ABA信号，从而停止对种子萌发和萌发后生长的抑制[46]。此外，在ABA存在下，PYR1抑制ABI1，释放ABI1阻断的AtSnRK2.6，导致效应蛋白高表达渗透响应15 (high expression of osmotically responsive 15, HOS15) 和AtSnRK2.6互作减弱，从而激活AtSnRK2.6 (图 2)。PYR1是ABA受体家族成员之一，在生物胁迫过程中转录上调并特异性感知ABA，启动ABA激活SnRK2介导的下游信号通路[38]。ABA与水杨酸(salicylic acid, SA) 和乙烯(ethylene, ET) 信号通路表现出复杂的拮抗和协同作用[47]。PYR1介导SA信号通路的激活则会削弱ET的感知，这对于激活真菌坏死生物的抗性至关重要[47]。此外，ABA与PYL的结合触发构象变化，使其结合并抑制PP2C，而PP2C抑制ABA信号[48]。总之，以上结果揭示了ABA信号终止的核心机制，这对植物应对不利环境和促进生长发育至关重要。
4 SnRK2的生物学功能SnRK2参与植物体内多种信号转导及生理代谢过程，如非生物胁迫、气孔运动、生长发育和病原体防御等。其通过调节一系列相关基因的表达，从而提高植物的抵抗能力，在植物生长发育和逆境胁迫应答过程中扮演着重要的角色。
4.1 SnRK2调节植物响应非生物逆境胁迫 4.1.1 SnRK2与植物耐盐性在盐渍条件下，植物体内大量积累的Na+和Cl–会使细胞内离子平衡紊乱，造成离子毒害和渗透胁迫，从而影响植物的生长和发育[49]。大量研究表明，SnRK2参与植物响应盐胁迫应答。例如，棉花GhSnRK2家族的5个成员(GhSnRK2.3、GhSnRK2.7、GhSnRK2.8、GhSnRK2.9和GhSnRK2.10) 在盐处理下表达水平显著上调[19]; 山茶树CsSnRK2s家族所有成员在盐胁迫下均有不同程度地被诱导[24]; 大豆GmSnRK2.1和GmSnRK2.2被高渗透胁迫诱导[50]，而GmSnRK2.3和GmSnRK2.4被高盐胁迫所诱导[51]; 马铃薯(Solanum tuberosum L.) StSnRK2.4也受盐处理的诱导和上调，并参与对渗透胁迫的响应[52]。笔者前期对甜菜BvSnRK2s在响应盐胁迫中的作用进行了深入研究，采用qRT-PCR技术对盐处理后的甜菜BvSnRK2s表达模式分析发现，甜菜叶和根中的BvSnRK2s不同程度地受盐胁迫的诱导和上调，表明BvSnRK2s在盐胁迫响应中具有潜在功能[6]。玉米ZmSAPK8在不同器官中均有所表达，且受到高盐胁迫的诱导; 过量表达ZmSAPK8的转基因拟南芥植株在盐胁迫下的种子萌发率、脯氨酸含量及存活率显著增加，而电解质渗透率降低，胁迫相关基因(RD29A、RD29B、RAB18、ABI1、DREB2A和P5CS1) 转录水平均有所提高，耐盐性较野生型显著增强[35]。然而，过量表达ZmSnRK2.11的拟南芥植株在盐胁迫下的相对含水量(relative water content, RWC) 降低，气孔关闭延迟，脯氨酸含量减少，丙二醛(malondialdehyde, MDA) 含量增加; 进一步发现，转基因植株ABI1和ABI2表达量增加，而DREB2A和P5CS1表达量降低[53]。由此可见，ZmSnRK2.11可能是一个参与植物盐胁迫信号转导通路的负调控因子。在拟南芥中过量表达CsSnRK2.5后，转基因植株的失水率下降，活性氧(reactive oxygen species, ROS) 和MDA含量减少，从而提高转基因植株的耐盐性[54]。在ABA处理下，毛果杨PtSnRK2s所有成员的转录丰度增加; 而在盐胁迫下，PtSnRK2部分成员被诱导[21]。进一步研究发现，在拟南芥中过量表达PtSnRK2.5和PtSnRK2.7，转基因植株在盐胁迫下保持较高的叶绿素和较长的根系，存活率也显著高于野生型植株[55]，表明过表达PtSnRK2s能够显著提高转基因植株的耐盐性。这些结果充分证明，SnRK2在植物响应盐胁迫中发挥着重要作用。
4.1.2 SnRK2与植物抗旱性干旱是制约植物生长和发育的另一个主要环境因素。近年来，SnRK2在植物抗旱性中的作用机制备受人们的关注。将苹果MpSnRK2.10转入拟南芥后发现，干旱处理野生型植株表现出严重萎蔫失水症状，而转基因植株仅表现出轻微的萎蔫症状; 值得一提的是，在恢复浇水后，转基因植株存活率高达77%–85%，而野生型植株只存活了50%。将该基因转入苹果后，转基因植株在干旱处理下的RWC高于野生型，ROS、MDA含量和能量损耗率(rate of energy loss, REL) 均低于野生型[56]。由此表明，过量表达MpSnRK2.10显著增强转基因植株的抗旱性。类似地，过量表达BdSnRK2.9、NtSnRK2.1和TaSnRK2.9转基因植株的抗旱性显著增强[15, 57-58]。此外，在拟南芥中过量表达TaSnRK2.3，使其在干旱胁迫下的水分保持能力(water retention ability, WRA)、叶绿素和脯氨酸含量均有所提高，其主根变长、侧根则变多[59]。可见，TaSnRK2.3是一种多功能调控因子，在作物育种中具有应用潜力。另外，对烟草NtSnRK2s第Ⅰ组成员进行了分析，发现NtSnRK2s对干旱胁迫的反应比对冷胁迫的反应快得多[57]，表明这些基因对干旱胁迫更为敏感。水稻OsSAPK2在干旱处理下表达水平显著上调; 与野生型相比，sapk2突变体对干旱胁迫和ROS更为敏感。进一步研究发现，OsSAPK2通过促进气孔关闭和上调胁迫响应及抗氧化酶相关基因的表达，提高ROS清除能力，以适应干旱胁迫[60]。最近研究发现，OsSAPK2可与OsbZIP23 (Oryza sativa basic leucine zipper 23) 和OsbZIP46相互作用并磷酸化其转录激活，过表达OsbZIP23增强了水稻对干旱胁迫的耐受性(图 2)[61-62]。过量表达OsSAPK9的转基因植株会引起一系列抗逆生理反应，如水分保持能力、可溶性糖和脯氨酸含量、膜稳定性和细胞解毒能力有所提高，从而提高转基因植株的抗旱性[63]。AtSnRK2.8的过表达也导致杨树对干旱胁迫的耐受性增强[64]。另外，过量表达SoSnRK2.1的转基因烟草在干旱胁迫下，其离子渗透(ion leakage, IL)、MDA和H2O2含量显著降低，而超氧化物歧化酶(superoxide dismutase, SOD)、过氧化酶(peroxidase, POD) 和过氧化氢酶(catalase, CAT) 活性显著增加[65]。最近研究发现，苦荞(Fagopyrum tataricum L.) 转录因子FtbZIP5受到FtSnRK2.6调控，可提高转基因拟南芥植株的抗旱性[66]。Zhu等发现周期蛋白依赖激酶(cyclin-dependent kinase, CDK8) 和SnRK2.6都与ERF/AP2 (ethylene responsive factor/apetala 2) 转录因子RAP2.6相互作用，正向调节干旱胁迫应答[67]。非生物胁迫反应RAF激酶(abiotic stress response RAF kinase, ARK) 在SnRK2介导的渗透胁迫应答中起至关重要的作用，其与SnRK2.6相互作用，SnRK2.6是干旱条件下气孔关闭的核心因子，以保护植物免受干旱胁迫伤害[68]。这些结果充分表明，SnRK2在调控植物响应干旱胁迫中起着至关重要的作用。
4.1.3 SnRK2与植物抗寒性当遭受低温逆境时，植物从感受低温信号到生理生化变化，再到基因表达调节，进而产生抗寒能力。大量研究表明，SnRK2参与调控植物响应低温胁迫。在低温处理下，水稻ossapk8突变体表现出生长缓慢、叶片泛黄及萎蔫等现象; 进一步发现，OsDREB1A、OsDREB1B、OsDREB1C和OsRAB21等基因的表达水平显著降低[69]。过表达TaSnRK2.3转基因拟南芥植株的存活率显著提高，抗寒性增强[59]。当冰叶草(Agropyron cristatum L.) AcSnRK2.11转入烟草后，转基因植株表现出更强的抗寒性，其存活率、RWC、叶绿素和可溶性糖含量均显著高于野生型[70]。此外，转基因植株的NtDREB1、NtDREB2、NtERD10A、NtERD10B、NtERD10C、NtERD10D、NtMnSOD、NtCDPK15和NtMPK9等基因转录水平也高于野生型[70]。这些结果表明，SnRK2作为低温胁迫响应信号通路相关的调节因子，可用于作物抗寒性遗传改良。
4.2 SnRK2调节植物响应生物逆境胁迫植物经常暴露在多种病原体下，依赖被动和主动防御机制来避免感染。病原菌通过分泌效应蛋白，抑制植物免疫反应系统，影响植物细胞的新陈代谢，从而促进病原菌感染[71]。植物免疫应答反应主要有ROS产生、胼胝质沉淀、MAPK激活，以及针对防御的基因转录重编程[72]。SnRK2参与免疫应答调节。Lee等利用无毒的Pst DC3000/avrRpt2 (Pseudo-monas syringae pv. tomato DC3000/avrRpt2) 细胞感染拟南芥植株并检测SnRK2转录水平，发现SnRK2.8在局部叶片中略微升高，在远端叶片中大幅增加[73]。这是由于拟南芥系统免疫需要SnRK2.8介导的发病机制相关基因非表达1 (nonexpresser of pathogenesis related genes 1, NPR1) 核输入(图 2)。由此证明SnRK2.8参与植物系统的免疫反应。将白叶枯病(Xanthomonas oryzae pv. oryzae) 菌株分别接种在OsSAPK9转基因株系和野生型株系，相比之下，转基因株系的病变长度(lesion lengths，LLs) 明显低于野生型，细菌生长量减少，表明OsSAPK9可能正向调控菌株对水稻白叶枯病毒的抗性[74]。拟南芥SnRK2.8与丁香假单胞菌(Pseudomonas syringae) AvrPtoB相互作用，从而抑制植株胼胝质沉积，可见SnRK2.8作为一种保守的植物激酶通过病原体效应物促进病害发生[75]。以上研究结果证明，SnRK2s参与调控植物对病原微生物的免疫反应。
4.3 SnRK2调节植物气孔运动气孔是植物叶片所特有的结构，在植物应对各种环境胁迫时，通过控制水分蒸腾、调节光合作用所需的气体交换发挥重要作用。ABA可促进气孔关闭、抑制光诱导的气孔开放[76]。SnRK2以ABA依赖的方式调节气孔运功。拟南芥AtSnRK2.6也被称为气孔开度1 (open stomata1, OST1) 或SRK2E，在ABA诱导的气孔关闭过程中起关键作用[77]。Yoshida等采用T-DNA插入法使SRK2E突变后，特异性地参与ABA依赖的气孔关闭; SRK2E能够与ABI1互作，在ABA诱导的气孔关闭过程中起关键作用(图 2)[78]。进一步分析表明，在气孔关闭过程中，升高的CO2和ABA信号相互作用，激发下游的OST1/SnRK2.6调控气孔运动[79]。Zhang等利用一种生物传感器SNACS (SnRK2 activity sensor) 观察到植物细胞中SnRK2对ABA的实时响应，证明了在气孔关闭过程中，SnRK2/OST1被ABA激活[80]。这些研究结果表明，通过激活SnRK2的活性来调控气孔运动，提高作物水分利用率，限制水分蒸发损失，以应对各种环境胁迫。
4.4 SnRK2调节植物生长发育 4.4.1 SnRK2调控种子萌发许多研究表明SnRK2调节植物种子萌发和休眠[81]。拟南芥AtSnRK2.2和AtSnRK2.3双突变体在种子萌发过程中对ABA不敏感，而单突变体表现出较强的敏感性，表明SnRK2.2和SnRK2.3是介导种子萌发过程中ABA信号转导的关键蛋白激酶[81]。类似地，AtSnRK2.6功能缺失致使突变体植株种子的油脂合成能力下降，而其过量表达则使转基因植株的蔗糖合成和叶片中脂肪酸去饱和能力增强，表明AtSnRK2.6在调控植物种子代谢稳态中具有重要作用[82]。最新研究发现，拟南芥BTB (broad-complex, tramtrack, and bric-a-brac)-A2s亚家族成员作为ABA信号强度平衡的负调控因子，通过降低AtSnRK2.3的活性来调控种子萌发过程中ABA敏感性[83]。SnRK2蛋白激酶在ABA介导的种子萌发抑制中发挥重要作用，ABA对水稻种子萌发的影响部分取决于茉莉酸(jasmonic acid, JA) 水平的升高，究其原因是ABA通过“SAPK10-bZIP72-AOC (allene oxide cyclase)”途径促进JA的生物合成，协同抑制水稻种子的萌发[84]。另外，激酶相关蛋白激酶(kinase-associated protein phosphatase, KAPP) 与SnRK2.2、SnRK2.3和SnRK2.6发生相互作用，且与ABA介导的种子萌发和幼苗早期生长呈负相关[85]。这些研究结果表明，SnRK2对植物种子的萌发和休眠起着重要的调控作用。
4.4.2 SnRK2调控根系发育SnRK2是植物根系发育的重要调控因子。过量表达TaSnRK2s使转基因植株的主根变长，对非生物胁迫的耐受性也显著增强[86]。在盐渍条件下，AtSnRK2.4和AtSnRK2.10可以迅速促进根系生长[87]。进一步研究发现，AtSnRK2.4与AtPP2C和AtABI1协同调控根系对盐胁迫的响应[88]。盐处理SnRK2家族第Ⅰ组成员都会促进主根的伸长，究其原因是SnRK2能和参与生长素合成的酶CYP79B互作，调控在盐胁迫下根系的生长和发育[89]。过量表达NtSnRK2.2使转基因烟草植株的可溶性糖积累增加，侧根变多、主根变长，根系发育状况变好[90]。这些结果表明，SnRK2参与调控植物根系的生长和发育。
4.4.3 SnRK2调控生殖生长SnRK2除了参与种子萌发和调控根系发育外，还参与调控其他一些生长发育，如开花、果实成熟、结籽等。苹果MdSnRK2.4和MdSnRK2.9可与调节乙烯合酶的转录因子MdHB1和MdHB2相互作用，通过磷酸化调控其转录活性及稳定性，从而促进乙烯的合成，影响果实的成熟[91]。TaSnRK2.3表达量与小麦植株株高、花序梗和倒数第二节长度以及千粒重显著相关[92]。水稻开花的关键调控因子OsbZIP77/OsFD1 (ferredoxins 1)，可被OsSAPK10磷酸化; 进一步研究发现，FACC-MADS15与bZIP77/FD1功能类似，OsSAPK10的过表达通过调控FACC-MADS15途径，使得植物提前开花[93]。此外，atsnrk2.2、atsnrk 2.3和atsnrk 2.6三重突变体幼苗表现出对ABA不敏感、结籽少、开花早等表型[94]。大豆GmSnRK2.2在幼苗、茎和荚果分裂和分生组织中表达丰度较高，而在种子中表达较低; GmSnRK2.16优先在花芽分化阶段的茎分生组织和叶芽中表达[9]。这些结果表明，SnRK2也参与调控植物开花、果实成熟、结籽等生殖生长和发育过程。
5 总结与展望迄今为止，SnRK家族已发现3个在植物代谢调控网络中起至关重要作用的亚家族SnRK1、SnRK2和SnRK3。SnRK1主要是糖信号转导过程中的关键因子，参与新陈代谢的调节，在激素和发育信号转导途径中起作用。SnRK2是植物中所特有的，受渗透胁迫和ABA诱导，对植物耐受环境胁迫方面具有重要作用。SnRK3也存在于植物中，可与CBLs相互作用，其作用主要集中在植物抵御逆境胁迫。
SnRK2激酶在植物响应生物和非生物胁迫以及生长发育中发挥着重要作用。迄今为止，对SnRK2作用机理的研究主要集中在ABA依赖的信号通路，对非ABA依赖信号通路研究相对较少，鉴于该信号通路对植物逆境胁迫有重要作用，未来还需深入研究。另外，SnRK2是信号级联的上游调控因子，轻微的转录改变可能会导致下游事件的发生，然而这方面的研究依然十分有限，仍需深入探究。随着生物信息学、高通量测序、过量表达、基因组编辑、RNA干扰等技术的发展，SnRK2激酶响应逆境胁迫的信号转导通路和作用机制将被进一步阐明，可为农作物抗逆性遗传改良提供基因优异资源与理论支持。
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