水稻同化物转运及其对逆境胁迫响应的机理∗

张彩霞，符冠富，奉保华，陈婷婷，陶龙兴

（中国水稻研究所/水稻生物学国家重点实验室，杭州 310006）

由于温室气体排放增多，全球极端气候频发，农作物产量及粮食安全受到严重威胁[1-4]。在某种恶劣条件下，单一胁迫可导致产量绝收[5]，加之耕地面积锐减，粮食安全问题日趋严峻[6-7]。水稻是世界最重要的粮食作物之一[8-11]，为满足人类对粮食日益增长的需求，预计到2035年，水稻产量与2010年相比需增加25%[12]。鉴于粮食安全隐患加剧及需求的增加，通过有效生产方式提高作物产量迫在眉睫[13-14]。产量形成与干物质积累、分配及转运密切相关，实质上是“源库流”协调统一的过程。“源”是制造或供应光合产物的器官，“库”是接受或积累光合产物的器官，“流”是指光合同化物从源到库的运输[15]。

光合同化物主要以蔗糖的形式通过韧皮部进行运输，即蔗糖装载进入小叶脉筛管分子后，经长距离运输进入库器官。适宜生长条件下，光合作用形成的碳水化合物大部分以非结构性碳水化合物形式暂时贮存在茎鞘中[16]，籽粒灌浆开启后，贮存于茎鞘中的同化物重新活化、装载进入韧皮部，最终运向籽粒。茎秆贮藏同化物及其向籽粒转运能力可能是影响作物高产的重要途径。因而，近年来作物单产难以提高甚至减产，极有可能与极端温度等逆境下同化物转运受抑有关。目前对“源”和“库”的研究较多，但对“流”的关注相对较少，尤其是逆境下同化物转运特征及响应机理。因此，本文在综述同化物运输和分配机理的基础上，明确植株对逆境胁迫的响应机制，重点分析同化物转运对逆境胁迫的响应机制，以期为提高水稻的稳产性和抗逆性提供理论参考，为未来粮食安全提供保障[17]。

1 水稻韧皮部同化物转运机理

1.1 同化物在叶片的装载

同化物在叶片的装载主要有两种途径，即质外体与共质体途径。质外体途径需要大量转运体的参与，例如 SWEET蛋白及蔗糖转运蛋白（sucrose transporter，SUT）[18-20]。一般情况下，SWEET蛋白将蔗糖分子运输到细胞壁，再由蔗糖转运蛋白（sucrose transporter，SUT）转运至筛管-伴胞复合体[18-20]。在同化物装载过程中，质膜上的 SUT是重要载体，装载的过程由质子动力势驱动[21]，主要负责蔗糖从“源”到“库”的质外体运输，并在蔗糖感应、“源”器官装载、韧皮部长距离运输和“库”器官卸载等过程中发挥重要作用[21]。目前水稻上已鉴定出 5个 SUTs基因，即 OsSUT1、OsSUT2、OsSUT3、OsSUT4和OsSUT5，仅OsSUT1和OsSUT3可能在质外体韧皮部装载中发挥作用[22-25]。OsSUT2主要作用于蔗糖从液泡到胞质的转运[26]，OsSUT3仅在花粉管中表达，在叶片装载中的表达很少[27-28]，而OsSUT4是一类低亲和性载体，主要与蔗糖在次生维管组织韧皮部中的装载有关[29-31]。鉴于此，OsSUT1可能是质外体韧皮部装载中最为重要的蔗糖转运体，因为已有研究表明，OsSUT1蛋白占主导地位，其表达主要集中在叶片和叶鞘韧皮部筛管和伴胞中[32]。然而OsSUT1基因敲除后，水稻营养生长未发生显著变化，但籽粒淀粉积累减少，结实率下降[33]，似表明OsSUT1蛋白表达受阻时，有另外的韧皮部装载途径代替或者弥补其功能，例如共质体途径[24]。

同化物的共质体装载是一个被动的过程，无需消耗能量，但需要叶肉细胞和韧皮部间有较高的浓度梯度及细胞间有发达的胞间连丝[34-35]。由于水稻叶片中有发达的胞间连丝，共质体装载途径可能起主要作用[36]。已有研究表明，蔗糖浓度与胞间连丝数量呈显著正相关关系，绝大部分具有高等或中等胞间连丝数量的植物均具有较高的蔗糖浓度[37]，而水稻叶片蔗糖含量明显高于拟南芥等质外体装载植物[38-41]。然而，还需要更多的生理和分子实验予以证明。近年来有学者提出一种特殊的共质体装载形式，即聚合物陷阱，通过消耗代谢能量将蔗糖转化成棉子糖、水苏四糖等低聚糖。低聚糖不能通过胞间连丝从筛管细胞扩散回叶肉细胞，但可以通过大的胞间连丝转入筛管细胞，从而维持韧皮部中高的糖浓度[19,36-37,42-43]。总之，植物同化物装载机制有很强的可塑性，会随着生长发育、生物和非生物胁迫以及不同基因型而发生改变[44-45]，在特定环境下采取的装载方式还需进一步探讨。

1.2 同化物在茎鞘韧皮部的运输

高等植物的韧皮部由一系列纵向排布的筛管分子、伴胞和薄壁细胞组成[46]。同化物在韧皮部中的运输速率不仅受到“源”端和“库”端压力梯度控制，还受到“源”中韧皮部装载速率和“库”中韧皮部卸载速率的调节。此外，筛管几何体结构也是影响同化物在韧皮部运输不可忽视的因素，尤其筛板孔形态特征。当筛管受损有汁液外流时，P蛋白就被定位于筛板孔，封堵筛分子以阻止汁液的进一步流失。长效解决筛管受损的机制则是在筛孔处产生胼胝质，即β-1，3-葡聚糖，由质膜中的胼胝质合酶合成并沉积于质膜和细胞壁之间[47]。Mullendore等[48]研究表明，植物在伤害条件下胼胝质几分钟内可把小筛板孔堵塞。当环境恢复正常后，胼胝质可在胼胝质水解酶介导下降解[47]。因此，筛管中的 P-蛋白及胼胝质等物质可堵塞筛板孔[49]，从而影响同化物运输。

植物营养生长阶段，叶片等同化器官产生的光合同化物主要贮存于茎鞘中，通过质外体或共质体途径卸载进入细胞后，以葡萄糖和果糖形式贮存于液泡中，当籽粒开始灌浆后，重新合成蔗糖装载进入筛管运往库器官。从茎鞘薄壁细胞重新装载回韧皮部的机理尚不清楚，既可能是共质体途径，也可能是质外体途径[43]。共质体途径同薄壁细胞与韧皮部筛管分子之间胞间连丝的数量、大小及是否通畅有关，而质外体途径主要受蔗糖转运体（SUTs）的影响[43]。Scofield等认为[33,50-52]，OsSUT1参与叶鞘储藏淀粉重新动员的同化物转运，而SUT2作为蔗糖信号感应器，在蔗糖转运等分子调控过程中发挥重要作用[53-54]。然而，有关茎鞘中同化物贮藏及转运的研究相对较少，还需要进一步探讨。

穗颈节间是“源”器官连接穗部的唯一通道，其结构特征与结实率、籽粒充实度和产量密切相关[55]。研究表明，水稻穗颈节间维管束数量对茎鞘非结构性碳化合物的转运具有显著的正向直接效应[56]。穗颈较粗、维管束数目多的品种，能够保持“流”的通畅，有利于提高同化物向籽粒转运的效率，从而提高收获指数[57]。于晓刚等[58]发现，颖果维管束可以通过调控同化物的运输与卸载影响颖果形成和稻米品质。然而，有关穗颈节间特征与同化物转运关系的研究较少，有待进一步深入研究。

1.3 同化物在颖果中的运输与卸载

韧皮部卸载是指韧皮部中同化物进入生长或贮藏组织的过程，包括同化物从筛管分子卸载和韧皮部后运输[59]。同化物通过叶、茎、穗轴、枝梗和小穗轴等维管系统向颖果输送，最终通过颖花背部维管束进入颖果。同化物在韧皮部中进行长距离运输后可通过质外体或共质体途径卸出，这两个途径可单独起作用，也可同时存在，不同发育阶段可采取不同的卸载途径[60-61]。在发育的种子中，母体与胚性组织间无胞间连丝，同化物必须经质外体途径卸载。尽管水稻光合同化物从背部维管束卸载后进入胚乳的途径存在争议，但有一点可以肯定，背部维管束和胚乳组织不直接接触，二者之间无共质体连通，但有珠心突起组织和质外体空间，由背部维管束运进颖果的同化物必须经过质外体后才能进入胚乳[62-63]。养分基本是按照小穗轴中央维管束—子房背部维管束—珠心突起—珠心层质外体—胚乳的路线进行运输的[64]。

在质外体卸载中，蔗糖由载体介导跨膜卸出到质外空间，一方面可被蔗糖转化酶分解为葡萄糖和果糖，然后由己糖载体吸收进入库细胞；另一方面可由蔗糖载体介导直接吸收进库细胞[65]。期间涉及3个过程，首先是蔗糖在转运体（SUTs）的作用下跨膜进入质外体，然后蔗糖被细胞壁转化酶（CINs）水解，最后在单糖转运体（MSTs）的作用下进入细胞[66]，表明SUTs、CINs和MSTs共同协调蔗糖的卸载过程。一般情况下，蔗糖转化酶活性在源（叶）中较低，有利于形成较高的蔗糖浓度以向贮藏器官转运，而在贮藏器官中较高，有利于蔗糖水解并转化为淀粉。

已经被鉴定出的5个蔗糖转运体中，OsSUT2、OsSUT3、OsSUT4和OsSUT5 mRNAs仅在开花时表达且仅维持到花后5d，而OsSUT1授粉后立即表达，并且持续到开花后25d[22,67]。此外，OsSUT1还参与了同化物跨过糊粉层运输到发育中胚乳的过程[33,63,67]。研究表明，OsSUT1水稻突变体的营养生长过程和野生型几乎没有区别[33,68]，敲除基因OsSUT1后叶片碳水化合物积累无变化，但水稻籽粒淀粉积累减少，结实率下降[33]。虽然这5种OsSUTs的表达及功能有所不同，但OsSUTs之间可相互协调，共同维持生物体的整个生命活动[22-25,26-31]。对于转化酶基因，研究表明CINs过量表达株系籽粒淀粉含量及粒重显著增加，目前已经有7个CINs被鉴定出，其中OsCIN1、OsCIN2、OsCIN4和OsCIN7在未成熟种子中表达，但作用时期不一致，表明这4个CINs基因都可能参与蔗糖卸载[69]。水稻中已经鉴定出 4个单糖转运体（MSTs），其中OsMST2、OsMST3和OsMST5属于糖转运体[70-71]。尽管水稻转运体表达特征已有研究，但其在水稻中表达活性与同化物卸载和产量形成的关系报道还较少，其具体功能还有待深入探讨。

另外还有研究表明，同化物从韧皮部的卸出与库端蔗糖酶及质膜H+-TP酶的活性密切相关[72]。同化物卸出到籽粒时，首先是质膜 H+-TP酶促进糖的逆化学势共转运，然后被转运的蔗糖在蔗糖酶的作用下被水解，从而维持筛管末端质外体空间较低的蔗糖浓度，防止其重新装载，同时蔗糖水解使质外体空间的水势降低，并促进筛管中糖和水的流出[72]。

2 水稻同化物转运对逆境胁迫的响应

2.1 高温热害

2.1.1 高温胁迫对水稻叶片装载的影响

如前所述，水稻光合同化物叶片韧皮部装载主要为共质体装载，叶肉细胞与筛管分子之间的胞间连丝数量、频率、大小及生理活性均可能成为限制同化物运输的因素。研究表明胞间连丝易受环境因素的影响，低温胁迫4h可观察到玉米叶片有胞间连丝关闭的现象，低温处理28h，叶片维管束鞘和维管薄壁细胞接口处的胞间连丝因胼胝质堵塞而关闭[73]。长时间的高温胁迫也可能会导致水稻叶片胞间连丝关闭，从而影响水稻同化物的装载，但类似的研究仍未见报道。虽然目前的研究表明质外体装载不是水稻叶片主要的装载方式，但在共质体装载受阻的情况下，质外体装载不失为一个很好的补充。这些蔗糖转运体基因（OsSUT1、OsSUT2、OsSUT3、OsSUT4和OsSUT5）表达可能会受到高温的抑制从而影响水稻同化物的装载。此外，装载过程由质子动力势所驱动[21]，如果高温导致植物体内代谢紊乱，不能形成正常的质子动力循环，势必引起装载紊乱。

高温导致水稻产量降低与籽粒充实度变差关系较大，因为同化物装载、运输及卸载中任意一个环节受高温逆境胁迫均可能导致蔗糖转运受阻，造成“流”的不畅。前期研究结果表明，高温条件下，无论是耐热性较强还是耐热性较差的品种，剑叶光合能力并未发生显著下降[74]，说明其光合同化物的合成在高温逆境中并未受显著伤害，因为叶片表面实际温度只有35℃左右[74]。因此推测高温对水稻同化物在叶片装载的影响较小，“流”的不畅可能主要与同化产物在茎鞘韧皮部运输及籽粒卸载有关。但由于胞间连丝超微结构及生理活性方面的研究还较薄弱，还有待进一步验证。

2.1.2 高温胁迫对同化物在茎鞘中运输的影响

目前，籽粒开始灌浆后光合产物从茎鞘薄壁细胞重新装载回韧皮部的机理还不清楚，但不论是共质体还是质外体途径均会受高温影响[43]。与叶片相比，高温下茎鞘和籽粒的散热能力较低，极易受高温伤害，气温40℃时，茎鞘和籽粒温度在38℃以上[74]。研究表明，植物受到高温胁迫时，胼胝质大量产生并在筛孔中沉积，几分钟内可以将筛板孔堵塞[48]。因此，高温逆境下筛板孔堵塞而引起“流”不畅的可能性较大，导致同化产物储藏于茎鞘薄壁细胞中[43]。逆境解除后，胼胝质在胼胝质水解酶的作用下降解，同化物可从薄壁细胞重新装载进入韧皮部筛管分子，随后运输至其它“库”组织[43]。然而，高温胁迫时间过长，胁迫强度超过临界值，胼胝质氧化酶可能受高温影响而导致活性降低甚至失活，阻碍胼胝质的降解，导致胼胝质始终沉积于筛板上，使茎鞘干物质量和可溶性碳水化合物含量在高温胁迫解除后仍呈增加趋势[43]。另外，高温下与蔗糖代谢、转运相关酶活性及相关基因表达受抑也可能是同化物转运受阻的主要原因。已有研究表明，高温等逆境可显著降低叶片及籽粒中蔗糖代谢及转运相关酶及基因的表达。然而，茎鞘中的这些酶及基因对高温响应的研究仍未见报道[75]。虽然灌浆结实期茎鞘贮藏同化物向籽粒转运是提高作物产量的有效手段，但有关茎鞘韧皮部装载与卸载方面的研究报道还较少，需要进一步深入探讨。

2.1.3 高温胁迫对同化物在颖果中运输及卸载的影响

水稻韧皮部同化物进入颖果需要以共质体途径经过颖果背部韧皮部，维管束薄壁细胞及珠心突起，然后再以质外体途径进入颖果背部糊粉层，最终进入胚乳细胞。研究表明，水稻受精后6d颖果背部维管束才能发育完整，因而此期发生高温胁迫不仅会影响颖果背部韧皮部、木质部、维管束薄壁细胞间胞间连丝的发育，还会影响背部维管束及胞间连丝的生理活性，从而阻碍光合产物及其它营养物质进入籽粒。更为严重的是高温还会导致颖果背部维管束早衰，严重阻碍同化物运输。高温不仅抑制背部维管束的发育，还可能影响颖果珠心及珠心突起的发育，不利于光合产物的卸载[62]。已有研究表明，珠心及珠心突起异常会导致灌浆速率降低，产量显著下降[76]。在质外体卸载阶段，同化物受SUTS、CINs和MSTs转运体共同调控。若高温抑制其活性及表达量，同化物卸载将受阻。研究表明，高温胁迫可显著降低籽粒中VIN活性，从而减少蔗糖向己糖的转化及胚乳中淀粉的合成[77]。此外，无论高温还是适温环境中，耐热性较强的植株幼嫩果实中 CWIN活性均显著高于耐热性差的品种[65,78-82]。

2.2 低温胁迫

众多非生物胁迫中，冷热害已成为水稻面临的主要气象灾害[83]，是制约粮食作物产量及地域分配的主要限制因素[84-85]。尽管全国大部分地区冷害的频率和强度有所下降，但阶段性和局地性的冷害仍有加重的趋势[86]。植物的起源地与其耐受低温冷害的能力关系密切[87-88]，水稻作为热带亚热带作物，对低温较敏感，通常气温降到4℃植株便会死亡[89]。将培养3周的水稻植株置于6℃条件下低温处理6h后叶片卷曲，恢复正常温度 24h后叶片展开[85]。研究表明，低温胁迫4h叶片有胞间连丝关闭的现象，28h叶片维管束鞘和维管薄壁细胞接口处的胞间连丝因胼胝质堵塞而关闭[90]。冷害胁迫韧皮部的瞬间堵塞可能是由于钙依赖封闭蛋白暂时性堵塞筛管引起的[91]。前人通过对植物茎进行局部低温处理，观察到叶片光合作用受抑，暗呼吸增强，韧皮部阻力增大，同化物转运受抑制[92]。通过对植物进行局部低温处理，研究结果表明低温处理上部组织碳水化合物积累，下部组织碳水化合物含量减少；低温处理部位上部韧皮部糖分侧漏增加，同时向下运输的碳水化合物减少，向根部运输的碳水化合物含量减少[93]。灌浆过程中低温逆境不仅导致植株净光合生产能力下降，同时也抑制了碳水化合物向韧皮部转运[94]，导致稻谷的充实度变差及品质变劣[95]。

2.3 干旱胁迫

水稻生长季节发生干旱胁迫将严重影响产量的形成[96-100]，尤其生殖生长期[101]。碳水化合物的转运和分配受水分影响，适度干旱胁迫能有效促进茎鞘中储藏的非结构性碳水化合物向穗部转运[102]。正常条件下茎鞘同化物对产量的贡献约为 20%，干旱胁迫下可提高至50%。该现象与气孔关系密切[103]，因为干旱下气孔导度降低，CO2吸收减少，作物光合产物生成受到限制，因而灌浆前茎鞘中贮藏的同化物成为籽粒灌浆的主要来源[104-106]。研究表明，ABA可加速灌浆进程，调用积累在茎鞘中的 NSC，促进积累同化物的再分配[107-108]。Travaglia等[109]研究表明，外源ABA可增加花期小麦碳水化合物积累并向籽粒转运，提高旱作小麦的产量。其原因主要是ABA提高细胞壁转化酶活性[110]，促进筛管分子运来的蔗糖分解为己糖，从而实现通过调节细胞壁转化酶的活性使“源”器官合成的同化物进入细胞壁空间，显著缓解源器官的压力[110]。

2.4 氮元素

作为水稻生长过程最重要的营养之一，氮的供应对水稻植株源库流关系影响甚大。氮供应不足时，叶面积指数过早下降，在籽粒灌浆时易产生源限制；长期低氮，植株的生长受到抑制，如分蘖发生停止，植株矮小。非结构性碳水化合物在植物体内积累是植物适应低氮条件的一种重要机制[111]。蔗糖在茎鞘韧皮部薄壁细胞合成果聚糖，维持蔗糖在源端与临时库端的浓度梯度，在籽粒灌浆期重新将积累的同化物输送至籽粒，从而补偿由于光合作用减弱造成的同化物积累不足[111]。然而，低氮能促进茎鞘碳、氮同化物的转运，与氮低效品种相比，氮高效品种抽穗后物质转运能力更强，氮素转运和氮素利用率更高[112-113]。增施氮肥可明显影响植株的蔗糖代谢，使蔗糖含量及合成能力提高，叶片碳氮同化物的转运量增加，但茎鞘碳氮同化物向籽粒的转运减弱[112]，主要是由于储存的碳为氮代谢提供碳骨架，从而构成很难再被释放的蛋白质或者氨基酸[114]。当氮供应过大时，茎秆生物量过量增加，叶片的正常衰老受到抑制，造成营养器官过度生长，茎秆伸长，根冠比下降，植株易倒伏，导致产量下降[115]。

3 研究展望

综上所述，无论正常或逆境条件下，同化物在叶片的装载、茎鞘中的运输及颖果的卸载均为影响水稻产量及品质形成的关键因素，尤其是同化物（蔗糖）在茎鞘中的储藏及再分配，然而高温等逆境条件下与糖转运蛋白相关的研究相对匮乏[116-119]。面对生态环境日益恶化及粮食需求急剧增加的困境[1-7]，加大对作物体内同化物代谢及转运的研究，并进行调控以实现逆境条件下稳产甚至增产的意义重大。虽然近年来，越来越多研究者认识到，“流”已经成为大穗型水稻进一步发展的限制因素，“流”的不畅不仅会限制产量潜力的发挥，还会影响稻米品质。然而，以往的研究多集中在以维管束为主的承载“流”组织的解剖、亚种间数量差异及遗传等方面，对流的质量研究较少，即对维管束的流量面积和“流”的生理活性，如胼胝质对流的影响、同化物的源端装载与库端卸出的酶和动力的研究较少，尤其在高温、低温及干旱等胁迫条件下，同化物在韧皮部的装载、运输及卸载特征更是少有报道。目前有关逆境胁迫对同化物转运影响的研究还有待完善，本文认为最主要的原因是受研究手段及技术所限。因此，新技术的开发应用可为该研究领域提供新的发展机遇，例如正电子发射动态放射性示踪技术（dynamic radiotracer imaging techniques using positron emission tomography），预测该技术的成功应用可弥补扫描电子显微镜、透射电子显微镜以及13C同位素示踪等研究方法的不足，成为探索逆境胁迫下同化物转运的强有力手段[120-122]。科学技术的进步，科研成果的日臻完善及科研水平的提高，可为该领域的研究提供更好的机遇，从而更好地造福人类。

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