Photosynthetic inorganic carbon utilization strategies and their ecological adaptability in aquatic plants
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摘要:
水生维管植物经历了从陆生向水生的“回归”演化,这个过程伴随着周围环境的一系列巨大变化,尤其是水体中无机碳环境与陆生生境的差异赋予了水生植物光合无机碳利用策略与陆生植物截然不同的生态学意义。本文综述了以光合作用为核心的水生植物无机碳利用策略的特殊性和多样性,以及研究水生植物无机碳利用策略的意义,并展望了基于水生植物尤其是水鳖科的无机碳利用策略为核心的植物适应机制研究的优势,旨在为水生植物适应机制和适应性进化研究提供新的思考方向。
Abstract:Aquatic vascular plants have undergone an evolutionary transition from terrestrial to aquatic habitats, necessitating substantial adaptations to their surrounding environments. In particular, the different inorganic carbon environments between underwater and terrestrial habitats confer distinct ecological significance to the photosynthetic inorganic carbon utilization strategies of both plant types. This paper elucidates the particularity and diversity of inorganic carbon utilization strategies in aquatic plants and the significance of these studies. In addition, the potential advantages in studying plant adaptation mechanisms based on inorganic carbon utilization strategies in aquatic plants (especially Hydrocharitaceae) is analyzed. Overall, this paper aims to provide a novel perspective for studying the adaptative mechanisms and evolutionary processes of aquatic plants, as well as new directions for research in this field.
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莲(Nelumbo nucifera Gaertn.)又称荷花,是莲科莲属的多年生水生植物。在被子植物系统发育群组(APG)中,莲科处于真双子叶的基部位置[1]。莲属仅由亚洲莲和美洲黄莲两个种组成。通常,莲主要是指亚洲莲。莲作为一种重要的水生经济植物,在中国已有两千多年的栽培历史[2]。在中国传统文化中,莲是高洁坚贞的君子象征,有诗文盛赞道,莲“出淤泥而不染,濯清涟而不妖”;在佛教文化盛行的东南亚国家,莲更是具有很高的宗教地位。不仅如此,莲还兼具食用和药用价值。莲藕和莲蓬都是深受大众喜爱的水生蔬菜。《神农本草经》和《本草纲目》中均记载道,莲的不同部位具有不同的药用效果。研究表明,莲叶具有抗病毒、抗肥胖的作用[3, 4];莲子具有抗氧化、抗癫痫的功效[5, 6]。
此外,莲还具有重要的观赏价值,是我国十大名花之一。荷花的花型和花色在很大程度上决定了其美学价值[7]。随着育种手段的多样化,荷花的花型得到了进一步丰富,现有半重瓣、重瓣、复瓣以及千瓣等花型分化[7]。在莲的两个种中,莲(即亚洲莲)的花色主要是白色系和红色系,而美洲黄莲则是黄色系。将莲与美洲黄莲进行杂交育种,涌现出大量花色艳丽的新品种。同时,还有一些花瓣呈现出“洒锦”样的条纹,即白色花瓣周边带不规则的紫红色条纹[8]。有意思的是,一些特殊品种,其花瓣还会产生“褪色”现象[9]。已有研究表明,莲的花色形成与花青素的积累呈正相关关系;而美洲黄莲的黄色积累与黄酮和黄酮醇有关,可能也受到胡萝卜素的影响[10]。本文将重点综述莲花瓣红色形成相关机理的研究。
由于其在植物抗逆、吸引传粉者等生理过程中的重要作用,以及其有益于人体健康,花青素的合成通路已在拟南芥(Arabidopsis thaliana (L.) Heynh.)等多种模式植物中得到广泛研究[11, 12]。研究表明,花青素合成途径属于类黄酮途径的一个分支,主要是由苯丙氨酸经过一系列的催化反应,生成无色的矢车菊素,再经过关键酶的催化作用生成有色的花青素,随后通过甲基化和糖基化修饰,最终生成稳定的花色苷[13]。花青素的合成不仅与通路中的重要结构基因有关,还受由MYB、b-HLH、WD40等3类转录因子形成的MBW复合体的调控,以及外界环境因素的影响[14]。
在模式植物中花青素的合成机制已经研究得较为透彻,但在莲中是否也存在相同的花青素合成途径和调控机制尚有待深入探讨。近年来,有关莲花色形成的机制已经有了较多报道。本文将从花瓣色素成分、花青素生物合成途径及分子调控机制入手,系统全面地综述有关莲花呈色分子机制的最新研究进展,以期加深人们对莲花呈色机理的认识,同时为以花色为目标性状的育种工作提供理论支撑和指导。
1. 莲花瓣中的主要色素
花朵颜色多样,其花瓣呈色与色素的种类和含量、液泡pH值、表皮细胞形状、色素与金属离子的络合形态等因素有关,其中最重要的是色素的种类和含量[15]。在自然界中,植物色素一般分为类胡萝卜素、甜菜碱和类黄酮等3类[16]。类胡萝卜素属于萜类化合物,是自然界中黄色和橙色的主要提供者,其含量的变化促进了万寿菊(Tagetes erecta L.)、金银花(Lonicera japonica Thunb.)、杏(Prunus armeniaca L.)等多种植物花色的动态变化[17-19]。甜菜碱是酪氨酸衍生的红紫色和黄色色素,储存在液泡中,目前仅在石竹目中发现[20]。类黄酮属于苯丙烷类的次生代谢物,具有从黄色到蓝色的广泛颜色范围。类黄酮种类繁多,根据其结构组成可分为花青素、黄酮醇、黄酮、黄烷酮、查耳酮等[21]。其中,花青素是广泛存在于植物中的水溶性天然色素。自然界中发现的花青素已多达上百种,其中,天竺葵色素(Pelargonidin,Pg)、矢车菊素(Cyanidin,Cy)、飞燕草色素(Delphinidin,Dp)、芍药色素(Peonidin,Pn)、牵牛花色素(Petunidin,Pt)和锦葵色素(Melvidin,Mv)等6种较为常见。花青素负责被子植物许多器官红色、蓝色和紫色的着色;而黄酮、黄酮醇则赋予植物从白色到淡黄色的颜色变化,并作为辅色素,调节一些蓝色和黑色花卉的花瓣色素沉积[22, 23]。
关于莲花瓣色素成分的研究十分丰富。早在2002年,Katori等[24]就用高效液相色谱技术(HPLC)分析了莲和美洲黄莲花瓣中的花青素和类胡萝卜素成分。结果发现,红色花瓣中具有5种花色苷,锦葵色素-3-O-葡萄糖苷占比最多;而在黄色、黄绿色和白色花瓣中未检测到花青素,但在黄绿色花瓣中检测到了少量的类胡萝卜素。随后,Yang等[25]通过将高效液相色谱-二级线性阵列检测器法和质谱法联用,实现了在40 min内同时检测莲花瓣中的花青素和黄酮醇,并在6种不同花色的花瓣中鉴定出了5种花色苷和10种黄酮醇苷,包括首次在莲中检测到的牵牛花色素和芍药色素。随着科学技术的发展,高效液相色谱-二级线性阵列检测器法和电喷雾质谱法联用(HPLC-DAD-ESI-MS)被认为是一种高效的类黄酮检测方法,Chen等[26]对类黄酮的提取方法进行了进一步优化,并利用该方法从莲花瓣中检测到了15种黄酮醇苷。次年,Chen等[27]在前期研究基础上,有针对性地优化了花瓣中花青素的提取条件和HPLC参数,并将莲与美洲黄莲的花瓣成分进行了比较。结果发现,美洲黄莲中含有丰富的黄酮醇,但未能检测到花青素;而莲中不仅含有丰富的黄酮醇,还含有大量的花青素。此外,Deng等[10]利用相同的提取和分析方法,鉴定了108个莲品种花瓣中的类黄酮成分和含量。结果显示,在不同花色的花瓣中,均可以检测到黄酮醇和黄酮,其中粉红色花瓣中的含量尤为丰富;在白色花瓣中未检测到花青素,在黄色和带有白色斑点的花瓣中检测到少量花青素;在红色系花瓣中均可以检测到5种花青素,其中,锦葵色素含量最多,飞燕草色素和牵牛花色素次之,矢车菊素和芍药色素最少,且在大多数情况下,花青素含量越高,花瓣颜色越深。后来,吴倩[28]利用超高效液相色谱-质谱联用技术(I-Class UPLC/Xevo TQ MS),建立了莲花瓣类黄酮的微量快速分析方法。由于检测灵敏度的提升,首次在白色花瓣中检测到了含量较低的芍药色素-3-O-葡萄糖醛酸苷。截至目前,共在莲花瓣中检测到9种花青素苷、26种黄酮醇苷和3种黄酮苷[29]。不同颜色花瓣的色素成分也大不相同。
2. 莲花青素合成途径
花青素是一类重要的植物次生代谢物,属于类黄酮水溶性天然色素。其生物合成途径在拟南芥、矮牵牛(Petunia hybrida Vilm.)、金鱼草(Antirrhinum majus L.)等模式植物中已研究得较为透彻[30-32]。一般而言,花青素合成途径分为3个阶段(图1)。第一阶段主要是由苯丙氨酸生成4-香豆酰辅酶A(4-coumaroyl-CoA),此阶段与植物的多种次生代谢途径共享。首先,前体物质苯丙氨酸在苯丙氨酸解氨酶(PAL)的作用下脱氨形成肉桂酸。随后,肉桂酸-4-羟化酶(C4H)将肉桂酸羟化生成香豆酸。紧接着,香豆酸在4-香豆酸辅酶A连接酶(4CL)的催化下生成4-香豆酰辅酶A。第二阶段主要是由4-香豆酰辅酶A生成二氢黄酮醇(Dihydroflavonol)、双氢槲皮素(Dihydroquercetin)和二氢杨梅黄酮(Dihydromyricetin),这三者均为花青素的前体物质。1分子的4-香豆酰辅酶A和3分子的丙二酰辅酶A在查尔酮合酶(CHS)的催化下生成该通路中的第一个类黄酮物质—柚皮素查尔酮(Naringenin chalcone)。然后,在查尔酮异构酶(CHI)和黄烷酮-3-羟化酶(F3H)的催化作用下,生成二氢黄酮醇。随后,类黄酮3’-羟化酶(F3’H)和类黄酮3’,5’-羟化酶(F3’5’H)分别在二氢黄酮醇的不同位点进行羟基化,生成双氢槲皮素和二氢杨梅黄酮。第三阶段主要是由花青素的前体物质生成各种花青素。二氢黄酮醇、双氢槲皮素和二氢杨梅黄酮在二氢黄酮醇4-还原酶(DFR)的作用下合成无色的天竺葵素、矢车菊素以及飞燕草色素,这些无色的花青素再在花青素合成酶(ANS)/无色花青素双加氧酶(LDOX)的催化下生成各种有色的花青素。最后在类黄酮葡萄糖基转移酶(UFGT)、酰基转移酶(AT)、甲基转移酶(MT)等酶的作用下形成稳定的花色苷。
图 1 花青素合成代谢通路PAL:苯丙氨酸解氨酶;C4H:肉桂酸-4-羟化酶;4CL:4-香豆酸辅酶A连接酶;CHS:查尔酮合酶;CHI:查尔酮异构酶;F3’H:类黄酮3’-羟化酶;F3’5’H:类黄酮3’,5’-羟化酶;DFR:二氢黄酮醇4-还原酶;ANS/LDOX:花青素合成酶/无色花青素双加氧酶;UFGT:类黄酮葡萄糖基转移酶;MT:甲基转移酶;AT:酰基转移酶;GST:谷胱甘肽巯基转移酶;CCR:肉桂酰辅酶A还原酶;FLS:黄酮醇合成酶;LAR:无色花青素还原酶;ANR:花青素还原酶。Figure 1. Anthocyanin biosynthesis pathwayPAL: Phenylalanine ammonia lyase; C4H: Cinnamate 4-hydroxylase; 4CL: 4-Coumarate coenzyme A ligase; CHS: Chalcone synthase; CHI: Chalcone isomerase; F3’H: Flavonoid 3’-hydroxylase; F3’5’H: Flavonoid 3’,5’-hydroxylase; DFR: Dihydroflavonol 4-reductase; ANS/LDOX: Anthocyanidinsynthase/ Leucoanthocyanidindioxygenase; UFGT: UDP-glycose flavonoid glycosyltransferase; MT: Methyltransferase; AT: Acyltransferase; GST: Glutathione S-transferase; CCR: Cinnamoyl-CoA reductase; FLS: Flavonol synthase; LAR: Leucoanthocyantin reductase; ANR: Anthocyanidin reductase.花青素合成的每一步生化反应都受到不同酶的催化,编码这些酶的基因被称为结构基因。根据结构基因在花青素合成途径中的位置,大致可将其分为早期结构基因(如CHS、CHI、F3H、F3’H)和晚期结构基因(如F3’5’H、DFR、ANS、UFGT)。虽然花青素的合成机理已在许多物种中研究得较为透彻,但莲的花青素合成调控的综合模型仍在初步建立阶段,仅有部分关键结构基因得到鉴定与研究。CHS是植物Ⅲ型聚酮合酶(PKS)超家族成员之一,是类黄酮合成途径中的第一个关键酶[33]。在许多物种中,CHS基因的表达水平与花青素的合成呈一定的正相关关系。莲的NnCHS与其他植物高度同源,且其表达量在红色花瓣中明显高于叶片[34]。沉默毛花猕猴桃(Actinidia eriantha Benth.)的AeCHS会降低其花瓣中的花青素含量,并使红色花瓣褪色成白色[35]。而在海棠(Malus spectabilis (Ait.) Borkh.)中过表达McCHS基因则会使之呈现更高的花青素含量以及更红的花瓣颜色[36]。CHI是第一个报道参与类黄酮生物合成途径的酶[37],广泛存在于植物和微生物中。Zhao等[38]分析了4个不同花色莲品种不同发育时期的NnCHI基因表达情况。结果表明,NnCHI基因一般在莲花发育早期阶段大量表达,而在花朵全盛时期,黄色品种的CHI含量显著高于其他颜色品种,说明该基因参与了黄酮和黄酮醇的合成。F3H是催化黄烷酮类化合物在C-3位置立体定向羟基化的关键酶,主要负责黄酮醇和花青素的生物合成[39]。F3H在类黄酮生物合成途径中的功能较为复杂,莲F3H基因与其他物种的同源性较低,可能具有物种特异性[38, 40]。相关研究显示,莲中NnF3H基因的mRNA表达水平和蛋白表达水平一致,均为红色花瓣低于白色花瓣,这可能与花青素的反馈调节有关,表明其不是花青素合成的限速酶[41]。ANS是2-氧戊二酸依赖的加氧酶家族的成员之一,负责催化无色花青素转变为有色花青素。因此,ANS基因的表达量在很大程度上决定了花青素的含量,ANS的功能缺失会导致花青苷无法形成[42]。Deng等[41]发现ANS在红色莲中的表达量高于白色莲,进一步分析发现,白色花瓣中基因的启动子区域具有较高水平的甲基化,阻碍了基因与转录因子的结合,从而降低了ANS的表达和花青素的积累。UFGT是莲中研究最多的结构基因之一,负责将不稳定的花青素转变为稳定的花青苷,利于细胞存储。Liu等[9]分析了‘秋三色’花瓣花青素含量在不同发育阶段的动态变化情况,发现从红色“褪色”到白色的过程中,花瓣的花青苷含量显著降低,同时,UFGT的表达量也逐渐降低。此外,Deng等[43]研究了红白嵌色莲‘大洒锦’的呈色机理,发现其花瓣红色区域含有丰富的花青苷,而在白色区域无法检测到花青苷。进一步研究发现,NnUFGT2蛋白在花瓣红色区域大量积累,而在白色区域快速降解,这可能是导致嵌色花瓣形成的关键因素。
3. 莲花青素合成的调控
由于花青素是一种次生代谢物,其合成往往在特殊的组织器官或特定的生理阶段(如响应生物胁迫和非生物胁迫)进行,因此,花青素的合成往往受到精确的调控。这种调控作用主要是由一系列转录因子来执行。花青素合成的调控方式具有物种特异性,由于调节机制的不同,植物得以形成纷繁复杂而各具特点的着色方式[44]。已有研究发现,拟南芥中花青素的早期生物合成结构基因受MYB转录因子的调节,晚期生物合成结构基因则受MBW复合体调控[45, 46]。而在玉米(Zea mays L.)中,花青素合成的结构基因均受MBW复合体的调控[47, 48]。这种调控方式的差异在其他双子叶和单子叶植物之间也普遍存在[49]。参与花青素合成调控的不同MYB转录因子能够促进或抑制MBW复合体的形成,或直接激活结构基因的转录[50, 51]。MBW复合体的作用方式在其他植物中已有研究。它既可直接作用于结构基因的启动子(如ANS),也可激活自身某个组成因子(如TT8和TTG1)的表达,还可以激活一些下游的转录因子(如GL3、GL2)[52]。
MYB类转录因子在多种植物的花青素合成调控中均起主要作用 [53, 54]。其高度保守的DNA结合结构域中包括3种不完全重复序列类型(R1、R2、R3),根据不完全重复序列类型和重复次数,可将MYB类转录因子分为4种类型,分别为MYB-related (1R-MYB)、R2R3-MYB(2R-MYB)、R1R2R3-MYB(3R-MYB) 和4R-MYB[55, 56]。1R-MYB通常包括一个或部分不完全重复序列类型,参与形态建成和次生代谢等生理过程[57]。CPC-like MYB(CPL)含有单个R3序列类型,属于1R-MYB分类,能够通过多种方式抑制花青素的合成[50]。R2R3-MYB作为植物中最大的MYB家族,已被证明参与苯丙烷代谢,且大部分成员对花青素的合成起正向调控作用,少部分起抑制作用[58-60]。3R-MYB往往在细胞周期调节中发挥作用[61]。4R-MYB是MYB家族中最小的一类,目前对其功能了解甚少[55]。在莲中,R2R3-MYB类转录因子NnMYB5已被确定为花青素合成的正向调控因子[62],通过增强谷胱甘肽巯基转移酶2基因(NnGST2)的表达来促进花青素向液泡的运输[63]。
转录因子bHLH (Basic Helix-Loop-Helix)在植物生长发育中起着重要作用,其结构域由大约60个氨基酸残基组成,分为两个保守基序,即1个基本区域和1个螺旋-环-螺旋区域[64]。在番茄(Solanum lycopersicum L.)、猕猴桃品种‘红阳’(Actinidia chinensis cv. ‘Hongyang’)、油菜(Brassica napus L.)等植物中已证实bHLH能够促进花青素的沉着[65-67]。NnTT8也属于bHLH转录因子,对莲中花青素的合成至关重要[68]。除了调节花青素的合成,bHLH还在调节种子的休眠和发芽、控制植物开花时间和环境响应等方面发挥重要作用[69-71]。
WD40转录因子也叫WD40重复蛋白,广泛存在于真核生物中。WD40结构域中含有大约40个保守的氨基酸残基,形成由7个重复叶片组成的β螺旋桨状结构,通常作为蛋白质-蛋白质或蛋白质-DNA相互作用的平台,在花青素合成调控中通过形成MBW复合体发挥作用[72, 73]。第一个调控花青素合成的WD40蛋白基因PhAN11是在牵牛花中被发现的,它能够促进花青素的积累[74],其同源基因的功能也在玉米和拟南芥中得到了验证[75, 76]。在水稻(Oryza sativa L.)和杨梅(Morella rubra Lour.)等植物中也有WD40转录因子被鉴定[77, 78]。但目前在莲中还缺乏对该基因的相关研究。
花青素在恶劣环境下能够为植物提供有效的保护。植物可以通过激素调节花青素的合成,从而实现对非生物胁迫的耐受性。研究表明,干旱胁迫能够提高植物中脱落酸的含量,增加MYB类转录因子的表达,从而促进果实或植株中花青素的积累,最终提高植物的抗旱性[79]。低温条件下,赤霉素的合成会减少,从而诱导花青素的积累以应对寒冷胁迫[80]。此外,环境条件也可以直接调节花青素的合成通路,如强光可以促进结构基因和调节基因的表达,弱光条件下,花青素结构基因的表达会下降甚至不表达[81]。研究发现,酸碱度会对莲花青素的积累产生影响,如褪色莲‘秋三色’中MBW复合体可通过控制质子泵相关基因的表达调节液泡pH值,从而影响花青素的合成[9]。
4. 总结与展望
莲具有极高的观赏价值、文化价值、生态环境价值、食用和药用价值,研究花色形成对于花莲的定向育种意义重大。针对莲不同品种的色素基本成分分析和鉴定的研究已十分丰富,对花青素合成途径中结构基因和调控基因的研究也取得了较大进展。但在莲花青素合成相关基因方面的研究成果仍然十分有限,目前仅鉴定了5个关键酶基因(CHS、CHI、F3H、ANS、UFGT)。对调控花色形成的具体分子机制的探究仍然不够深入,且在模式植物中推定的花青素合成调控路径也未得到验证。
目前,莲全基因组的二代和三代测序工作均已完成,多个版本的基因组组装序列和注释已经发布,这为莲功能基因组学和分子育种研究提供了丰富的基因资源。然而,由于缺乏稳定的遗传转化体系,相关基因的功能验证无法在莲中开展,莲遗传转化体系屏障的突破将会为相关研究提供支持。
借助人工杂交育种手段,现已培育出许多荷花新品种。但亚洲莲的花色依旧相对单调,仍然局限于红色系和白色系,尚未培育出蓝色、橙色等新颖花色。在莲中建立完善的色素形成通路后,结合新型基因编辑工具,靶向改造相应的结构基因,将有望培育出具有突破性的花色新品种。
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图 1 水生植物无机碳利用策略的特殊性和多样性
A:中华水韭(Isoetes sinensis Palmer);B:龙舌草(Ottelia alismoides (L.) Pers.)(照片由付文龙拍摄);C:水筛(Blyxa japonica (Miq.) Maxim.);D:穿叶眼子菜(Potamogeton perfoliatus L.);E:一种轮藻(Chara sp.)(照片由刘洋拍摄);F:眼子菜(Potamogeton distinctus A. Bennett);G:紫萍(Spirodela polyrhiza (L.) Schleid)。轮藻不属于植物,但在无机碳利用时,通常将其视为沉水植物。图中pH极性叶片染色显示眼子菜属植物近轴面被酚酞染成红色(碱性),远轴面无色,表明这类叶片在利用HCO3−过程中形成pH极性。溴麝香草酚蓝染色显示轮藻属在利用HCO3−过程中,细胞呈酸性(黄色)和碱性(蓝色)相间(图片来源于Beilby等[57])。
Figure 1. The distinctiveness and diversity of inorganic carbon utilization strategies in aquatic plants
A: Isoetes sinensis Palmer; B: Ottelia alismoides (L.) Pers. (Photographed by Fu Wenlong); C: Blyxa japonica (Miq.) Maxim.; D: Potamogeton perfoliatus L.; E: Chara sp. (Photographed by Liu Yang); F: Potamogeton distinctus A. Bennett; G: Spirodela polyrhiza (L.) Schleid. Characean algae are not plant, but they are usually regarded as submerged plants in study of inorganic carbon utilization. Under phenolphthalein staining, the adaxial surface of Potamogeton plant leaf is red (alkalinity), while the abaxial surface is colorless, indicating pH polarity of two sides of the same leaf during the process of HCO3− use. Under bromothymol blue staining, the interior of Chara cell exhibits alternating acidity (yellow) and alkalinity (blue) during HCO3−use (The image is from Beilby et al. [57]).
表 1 植物在水生环境中面临的机遇和挑战及水生植物的应对方式(改自Maberly 和 Gontero[14])
Table 1 Opportunities and challenges faced by plants in aquatic environments and how aquatic plants respond (modified from Maberly and Gontero[14])
环境特征
Environmental feature机遇
Opportunity挑战
Challenge水生植物应对方式
Aquatic plant response水分可利用性高 无水分胁迫 藻类竞争 生产力高;表皮细胞包含叶绿体;
叶片薄;分泌化感物质生长介质密度高 支撑性高 水阻力大 机械组织投资减少;茎和叶具有韧性 光照可利用性低 光抑制和光伤害可能低 光合作用和分布深度受限 表皮细胞富含叶绿体 温度变化幅度小 温度胁迫风险小 无 无 O2可利用性低 光呼吸可能低 地下组织器官缺氧 通气组织贯通根茎叶;向地下部位泵氧 无机碳可利用性低 局部生境CO2多;
HCO3−浓度高CO2日变化和年变化
范围极大拓展到局部高CO2生境生长;发展无机碳浓缩机制:HCO3−利用、C4和景天酸代谢(CAM) 养分可利用性高 根、茎、叶均可接触营养元素 藻类竞争 根茎叶均吸收养分;化感作用 表 2 水鳖科植物无机碳利用策略的多样性
Table 2 Diversity of inorganic carbon utilization strategies in Hydrocharitaceae plants
属
Genus种数
No. of speciesHCO3−利用
Bicarbonate use大气CO2
Atmosphere CO2基质CO2
Substrate CO2C4途径
C4 pathwayCAM途径
CAM pathwayAppertiella 1 U U U U U Blyxa[50, 56] 14 N N S N N Elodea[50, 75] 9 Y N U I/N N Enhalus[76] 1 Y N U U U Halophila[77] 17 Y N U N N Hydrilla[78, 73] 1 Y N U I S Hydrocharisa 5 N Y U U U Lagarosiphon[50] 9 Y/N U U U U Najas[50] 39 Y/N N U N N Nechamandra[56, 79] 1 Y N U U S Ottelia[45, 79-81] 23 Y Y U Y/N I/N Stratiotes[82] 1 Y Y U U U Thalassia[77,83,84] 2 Y N U S N Vallisneria[56, 84] 14 Y N Y N S/N 注:Y,具备该途径;N,不具备该途径;S,疑似具备该途径;U,尚未进行测试;I,需要在特殊条件下诱导出该途径;Y/N,在已测试的该属所有物种中,有的物种具有该途径,有的物种不具有该途径;I/N,在已测试的该属所有物种中,有的物种该途径的产生需要诱导,有的物种则不具备该途径;S/N,在已测试的该属所有物种中,有些物种疑似具有该途径,有的物种不具备该途径。a,数据来源于本实验室。 Notes: Y, all plants have this pathway; N, none plant have this pathway; S, the plants are suspected to have this pathway; U, not yet tested; I, this pathway needs to be induced under special conditions; Y/S, among all the tested species from this genus, some have this pathway and some do not; I/N, among all the tested species from this genus, some need to be induced to produce this pathway and some do not have this pathway; S/N, among all the tested species from this genus, some are suspected to have this pathway and some do not have. a, indicates the data are from our lab. -
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