低磷胁迫对玉米磷吸收、转运及IAA和CTK水平与分布的影响
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摘要
磷素作为植物生长发育所必需的大量元素之一，不仅是植物细胞的结构成分，而且在细胞的代谢调控及信号转导中起重要作用。由于磷素在土壤中的相对不可移动性，土壤有效磷不足成为限制植物生长和产量的主要因素之一。为应对土壤低磷，植物已进化出低磷耐受机制，在根系结构、磷吸收和体内磷周转利用等方面做出适当调整，以更好地适应低磷环境。近年来，植物磷吸收调节的研究已取得了一定的进展，但有关于磷吸收与体内磷浓度之间的关系仍有待于进一步研究；对于低磷状况下叶细胞的磷吸收动力学特性及其生理意义也有待于揭示：对植物激素在植物低磷反应中作用的认识也需要拓宽和深入。本工作以玉米自交系Qi319为材料，分析了植株的磷吸收与体内磷浓度之间的关系；研究了低磷条件下成熟叶的细胞磷吸收动力学特征的变化，进而探讨了该变化在叶片磷输出转运中的生理学意义；比较了Qi319与其衍生的耐低磷自交系99037在不同供磷条件下的根系构型和根部IAA、玉米素的水平与分布，观察了外源激素和化学抑制剂对根系构型的影响，进一步揭示了玉米磷吸收、转运的调控机制，以及激素在低磷诱导的根系构型改变中的作用。
一、玉米根系磷吸收的调节
1．植株磷吸收状态与体内磷浓度之间的关系
将Qi319植株在不同供磷条件(0．1-1000μM KH_2PO_4)下进行溶液培养25天，分析植株的供磷水平、体内磷浓度与磷吸收之间的关系。结果显示，植株的体内磷浓度随供磷水平的提高而增大，磷吸收速率(V_(max))和对磷(phosphate，Pi)的亲和力则随供磷水平的提高而减小。相关性分析表明，在0．1-1000μM供磷范围内，磷吸收表观V_(max)值与供磷水平、茎叶及根部磷浓度呈显著负相关(P<0．01)，在75-1000μM的供磷范围内，表观K_m和C_(min)值与供磷水平、茎叶及根部磷浓度呈显著正相关(P<0．01)。当供磷水平处在0．1至75μM之间时，表观K_m和C_(min)加值变化不显著(p>0．05)。偏相关性分析显示，植株的磷吸收V_(max)、K_m和C_(min)值与体内磷浓度显著相关(P<0．01、P<0．05、P<0．05)，而与供磷水平之间无显著的相关性(P>0．05)。这些结果表明植株的磷吸收状态与体内磷浓度具有密切的关系。
在含1000μM KH_2PO_4的营养液中培养23天后，Qi319植株转入无磷营养液中继续培养10天，观察缺磷胁迫期间植株的体内磷浓度和磷吸收的变化。结果显示，随缺磷胁迫时间的延长，植株的体内磷浓度逐渐降低，而磷吸收V_(max)和对Pi的亲和力则逐渐增大。相关性分析表明在缺磷胁迫期间植株的磷吸收V_(max)、K_m和C_(min)值与茎叶及根部磷浓度之间也存在显著相关性(P<0．01)。
对在无磷营养液中生长的玉米植株进行叶面供磷处理3天，发现植株的体内磷浓度逐渐升高，且茎叶与根部磷浓度存在较大差异。当茎叶磷浓度已达足磷水平时，根部磷浓度虽有所增加，但仍处在严重缺磷状态，而此时植株的根系磷吸收表观V_(max)值和对Pi的亲和力显著减小(P<0．01)。上述结果表明，叶面供磷处理植株的根系磷吸收与茎叶磷浓度有关，这为系统磷信号调控根系磷吸收的观点提供了新证据。
2．依据茎叶磷浓度估测植株的磷吸收状态
玉米植株磷吸收动力学参数与体内磷浓度之间存在着显著的相关性，预示着可依据体内磷浓度来估测玉米植株的磷吸收状态。本研究对玉米植株的磷吸收动力学参数(V_(max)、K_m和C_(min))与茎叶磷浓度进行线性回归分析，得到三个具有较高拟合优度(R~2)的线性方程式。利用这三个方程式，依据茎叶磷浓度估算不同磷处理植株的磷吸收动力学参数，并与传统的离子耗竭法测定的参数值相比较。结果显示，除缺磷预处理植株在恢复供磷后的几天内，V_(max)的估算值比离子耗竭技术的测定值偏低外，不同磷处理植株的磷吸收动力学参数(V_(max)、K_m和C_(min))的估算值均与离子耗竭法的测定值相吻合。以上结果表明，玉米茎叶磷浓度可反映根系的磷吸收状态，因此，依据茎叶磷浓度估算根系磷吸收动力学参数可成为一个方便快捷的估测玉米植株磷吸收状态的新方法，该方法对指导玉米精准化施用磷肥和玉米高产有一定意义。
二、低磷胁迫对玉米成熟叶磷转运的影响
用含1000μM KH_2PO_4营养液培养23天的Qi319植株移入低磷(0．1μM Pi)营养液后(0-14天)，检测茎基部和成熟叶叶片木质部伤流液的Pi浓度，以及成熟叶叶片韧皮部渗出液的磷含量，来反映成熟叶的磷输入和输出的变化。结果显示，在低磷条件下，通过木质部向成熟叶输入的磷明显减少，通过韧皮部输出的磷则相对增多。
用成熟叶制备质膜囊泡进行磷吸收测定，发现来自于低磷处理植株质膜囊泡的磷吸收表观V_(max)值，与来自高磷对照植株的相比显著增大(P<0．01)，表明成熟叶的细胞磷吸收能力在低磷胁迫下明显增强。为探究该动力学特征变化的生理意义，在成熟叶的叶片上局部施加含NEM(跨质膜磷转运抑制剂)或不含NEM的~(32)P标记Pi溶液，检测叶片(去除Pi施用区域)和叶片韧皮部渗出液的放射活度，结果显示，在NEM存在时，叶细胞从质外体中吸收~(32)P标记Pi的量显著减少(P<0．01)，叶片韧皮部渗出液的放射活度也显著降低(P<0．01)，这表明叶细胞从质外体中吸收Pi与叶的磷输出有关。玉米成熟叶的细胞在低磷胁迫下增强磷吸收能力，可能有利于从低Pi浓度的质外体及木质部中吸收较多的Pi，这对维持细胞的正常生理活动和增加叶的磷输出具有一定的意义。
三、生长素和细胞分裂素在低磷诱导的根系构型改变中的作用
植物根系的胚后发育是高度可塑的，植物通常通过调控根系的胚后发育和修饰根系构型以更好地适应外部环境。在自然生态系统中，有效磷不足是限制植物生长的重要因素之一，而植物对磷养分的吸收能力与根系构型密切相关。植物激素，如生长素和细胞分裂素都参与根系的胚后发育调控和构型修饰，但这两种激素及其之间的互作在低磷诱导的根系构型改变中的作用目前仍了解甚少。
自交系99037是通过细胞工程技术获得的、来自于Qi319的耐低磷细胞突变体。在不同供磷条件下，99037植株较Qi319有更长的轴根(基根和不定根)和侧根以及更高的磷吸收累积能力；在田间99037植株也比Qi319具有更高的干物质和籽粒产量。
将99037和Qi319植株在高磷(1000μM Pi)或低磷(5μM Pi)营养液中培养18天，观察低磷胁迫下根系IAA和玉米素水平与分布及根系构型的变化。结果显示，在低磷条件下，玉米素浓度在植株的轴根幼嫩区段(约1 cm)和成熟区段(去除轴根幼嫩区段)以不同的幅度显著降低(P<0．05)，IAA浓度及其与玉米素浓度的比值在轴根幼嫩区段明显增大，在轴根成熟区段却显著减小(P<0．05)；同时在低磷条件下，植株的轴根数目、侧根平均长度和密度比在高磷条件下显著减少(P<0．05)，而轴根平均长度却显著增加(P<0．05)，因而形成了轴根长的根系。上述结果提示，在低磷条件下，玉米植株根系的构型发生改变，与生长素和玉米素在根部的水平和分布以及两种激素浓度比例的变化有关。
为进一步验证，本工作用6-BA和NAA单独或组合处理以及用生长素极性运输抑制剂(TIBA)处理不同供磷条件下生长的两个自交系植株，观察根系结构的变化。结果支持了上述推测。
99037和Qi319植株在根系结构、根系IAA浓度和分布、IAA与玉米素浓度比例、以及其侧根对低磷胁迫和TIBA的敏感性等方面存在差异，这些差异及差异间的对应关系也支持上述推测。
基于以上结果可以认为，在低磷条件下，生长素和细胞分裂素在玉米根系中的浓度和分布及两种激素的浓度比例发生明显的变化，这些变化以及两种激素间的互作在低磷诱导的根系构型改变中起着重要作用。寻找玉米磷信号和激素信号网络的共有接点无疑会加深对玉米耐低磷机制的认识。
As an essential macronutrient for plant growth and development, phosphorus (P) not only is an important architectural component of plant cells, but also plays an important role in cell metabolism and signal transduction. However, low availability of phosphate (Pi) in soil has become a major constraint for plant growth and production, due to its low immobility. To adapt the low-P conditions, plants have evolved complex strategies including modifications of root architecture, improvement of Pi acquisition and recycling etc. In recent years, some progress has been made in the studies on regulation of Pi uptake in plants. Nonetheless, the relationship between Pi uptake and internal P concentrations (IPCs) of plants needs to be further explored; kinetic characteristics of Pi uptake by cells of mature leaf under low P stress and its physiological significance remain to be discovered; and knowledge concerning the role of phytohormones in low-P response of plants remain to be elucidated. In the present work, using maize (Zea mays L.) inbred line Qi319, the relationship between Pi uptake and IPCs of plants was analyzed, changes of kinetic characteristics of Pi uptake by cells of mature leaf under P deficiency were studied, and the physiological role of these changes in leaf P output was discussed. Furthermore, root architectural characteristics, levels and distribution of endogenous auxin and cytokinkin within root system, and effect of exogenous phytohormones and chemical inhibitor on root architecture were investigated in seedlings of Qi319 and 99037 (a low P-tolerant line derived from Qi319) under different P conditions. The objective of the present study is to reveal regulation mechanisms of Pi uptake and transport, and the role of auxin and cytokinnin in the low-P-induced alterations of root architecture in maize.
1. Regulation of Pi uptake by maize roots
(1) Relationship between Pi uptake and internal P concentrations of plants
Seedlings of maize imbed line Qi319 were grown under different P supplies (0.1-1,000μM KH_2PO_4) for 25 days, and the relationship among P supply level, IPCs, and Pi uptake of plants were investigated. The results indicated that IPCs of the plants increased with the elevation of P supply level, whereas Pi uptake rate (V_(max)) and affinity for Pi of the plants reduced. Correlation analysis showed that apparent V_(max) value of Pi uptake was reversely related to external P concentrations (EPCs), shoot and root P concentrations (SPCs and RPCs) of the plants within the entire P supply range (0.1-1,000μM) (P < 0.01). Among the P supply range from75μM to 1,000μM apparent K_m and C_(min) values of Pi uptake were positively related to EPCs. SPCs and RPCs respectively (P < 0.01). As P supply level ranged from 0.1μM to 75μM, there was no significant changes in K_m or C_(min) values. Partial correlation analysis revealed that these parameters (V_(max), K_m and C_(min)) were only significantly correlated with SPCs and RPCs (P < 0.05), not EPCs (P > 0.05). Taken together, these results showed that Pi uptake by roots had a close relationship with the IPCs.
Qi319 seedlings grown in nutrient solution containing 1,000μM KH_2PO_4 for 23 days were deprived of Pi for 10 days, and variations of IPCs and Pi uptake during P deprivation were investigated. The results indicated that SPCs and RPCs gradually decreased with the prolongation of P deprivation period, while affinity for Pi and Pi uptake rate (V_(max)) of the plants increased continually. Furthermore, significant correlations were also clearly showed between the parameters (V_(max), K_m and C_(min)) and IPCs of shoots and roots in the phase of P deprivation (P < 0.01).
Seedlings of Qi319 grown in nutrient solution without P were supplied with Pi through leaves. It was observed that within 3 days of the P recovery period, IPCs of the plants increased gradually. However, difference in IPCs between the shoots and roots was considerable: the SPCs had increased to a sufficient P level, while the RPCs, though increased at some extent, were still under severe P deficiency. Meanwhile, both Pi uptake capacity (V_(max) and affinity for Pi of roots in these seedlings decreased significantly compared to those without P supply (P < 0.01). These results showed that the Pi uptake status of roots have a relationship with SPCs of the plants in this P recovery period, and provided compelling evidence for the hypothesis that systemic P signal regulates Pi uptake of roots.
(2) Estimation of Pi uptake status according to SPCs of maize plants
Significant correlation between IPCs and parameters of Pi uptake kinetics suggested that Pi uptake by maize plants could be estimated by IPCs. In the present study, three equations with high determinants of coefficient (R~2) were obtained based on the linear regressions of the kinetic parameters and SPCs. With these equations, values of K_m, C_(min) and V_(max) of Pi uptake by seedlings grown in different circumstances were calculated by SPCs and compared with the values determined by Pi depletion technique. For V_(max), there was a parallel relationship between the values estimated by SPCs and determined by Pi depletion technique, only except the period of resupplying Pi to the Pi-starved seedlings over several days. For K_m and C_(min). the values estimated by SPCs were consistent with those obtained from Pi depletion experiments. These results indicated that SPCs basically reflect the status of Pi uptake of plants in a linear manner, and it is possible to estimate the Pi uptake kinetic parameters according to SPCs, which is potential to be a novel and convenient method for estimating the Pi-uptake status of maize plants. This method would be helpful for applying P fertilizers finely and economically and achieving high yield of maize.
2 Effect of low-P stress on P transport in maize mature leaf
(1) After grown under 1000μM KH_2PO_4 for 23 days, Qi319 seedlings were treated under low P (0.1μM Pi) condition (0-14 days), and Pi concentrations of stem and mature leaf xylem saps as well as P contents of mature leaf phloem exudates were monitored. The results indicated that P which was imported to mature leaf through xylem decreased, whereas P output of the leaf through phloem was enhanced relatively under low-P conditions.
(2) Pi uptake assay with plasma membrane vesicles revealed that apparent V_(max) value of Pi uptake by plasma membrane vesicles which were prepared from the mature leaves of seedlings treated under low P condition was greater than those of the control plants (P < 0.01). The result indicated that Pi uptake by cells of mature leaf was enhanced under P deficiency. To explore the physiological significance of variations of Pi uptake by cells of mature leaf under P deficiency, the maize mature leaf was applied locally with Pi solutions labeled by ~(32)P in the presence or absence of an inhibitory agent (NEM) for Pi transport across plasma membranes; and then, radioactivity of the leaf (laminas where ~(32)P was applied were cut out) and leaf phloem exudates were measured. The results indicated that in the presence of NEM, ~(32)P labeled Pi uptake by the leaf cells from leaf apoplasts was inhibited significantly (P< 0.01), and synchronously, radioactivity of the leaf phloem exudates decrease significantly compared with that in the absence of NEM (P < 0.05). showing a relationship between Pi uptake by leaf cells from apoplasts and P export of the leaf. Taken together, it could be concluded that under low-P stress capacity of Pi uptake by cells of mature leaf was enhanced, which would benefit leaf cells to absorb Pi from leaf apoplasts (including xylem apoplasts), and maintain the normal physiological activity of the cells and increase the P export of mature leaf.
3 Roles of auxin and cytokinin in the low-P-induced alterations of root architecture
The postembryonic developmental program of plant root system is plastic, allowing changes in root architecture to adapt to environmental conditions including P availability. Insufficient of available Pi in soil is one of the important factors that strongly limit plant growth. Root architecture, to some extent, determines the capacity of plant Pi acquisition. Phytohormones, such as auxin and cytokinin, involve in the postembryonic development of root system, however, the roles of both hormornes and their mutual interaction in the low-P-induced alterations of root architecture have been unclear so far.
The inbred line 99037 is developed from Qi319 by cellular engineering. Under different P supply levels, 99037 plants have longer lateral and axile roots (including primary and adventitious roots) and higher capacity of P uptake and accumulation than Qi319. In the field experiments, both total dry weight and seed yield of 99037 are greater than those of Qi319, respectively.
Seedlings of 99037 and Qi319 were grown hydroponically under low (LP, 5μM Pi) or high (HP, 1,000μM Pi) P conditions for18 days, and the root architecture and levels and distribution of IAA and zeatin within root system were investigated. The results showed that under LP, zeatin concentrations in both young segments of axile roots (1 cm long from apex, YSARs) and mature segments of axile roots (behind YSARs) decreased (P < 0.05) compared to those under HP; IAA concentrations and the ratio of IAA to zeatin (IAA concentrations/zeatin concentrations) increased markedly in YSARs under LP, while reduced significantly in MSARs (P < 0.05), compared to those under HP. Synchronously, the number of aixle roots, and the density and average length of lateral roots decreased significantly (P < 0.05), whereas average length of axile roots increased significantly (P < 0.05) under LP, compared to those under HP. These results indicated that root architecture, levels and distribution of auxin and zeatin as well as the ratio of IAA to zeatin within root system were altered notably under LP, implying that variations of levels and distribution of IAA and zeatin as well as their mutual interaction within root system played roles in the low-P-induced alterations of root architecture.
To validate this presumption, seedlings of both lines grown under LP or HP were treated with 6-BA and NAA solely or together, or an auxin porlar transport inhibitor (TIBA), and the alterations of root architecture of the plants were investigated. The results supported the presumption that variations of levels and distribution of auxin and cytokinin as well as interaction between them within root system played roles in alterations of root architecture under low-P conditions. In addition, this presumption was further supported by the differences in root architecture, level and distribution of IAA, ratio of IAA to zeatin, and the resistence of lateral roots to low-P stress and TIBA between 99037 and Qi319 root systems.
In summary, levels and distribution of auxin and cytokinin as well as the ratio of both within root system vary notably under LP condition. And these variations and interaction between the two hormones play an important role in the low-P-induced alterations of maize root architecture. Seeking the cross-talk of phytohormone and phosphorus signaling network may help to understand the low P tolerance mechanism in maize.
一、玉米根系磷吸收的调节
1．植株磷吸收状态与体内磷浓度之间的关系
将Qi319植株在不同供磷条件(0．1-1000μM KH_2PO_4)下进行溶液培养25天，分析植株的供磷水平、体内磷浓度与磷吸收之间的关系。结果显示，植株的体内磷浓度随供磷水平的提高而增大，磷吸收速率(V_(max))和对磷(phosphate，Pi)的亲和力则随供磷水平的提高而减小。相关性分析表明，在0．1-1000μM供磷范围内，磷吸收表观V_(max)值与供磷水平、茎叶及根部磷浓度呈显著负相关(P<0．01)，在75-1000μM的供磷范围内，表观K_m和C_(min)值与供磷水平、茎叶及根部磷浓度呈显著正相关(P<0．01)。当供磷水平处在0．1至75μM之间时，表观K_m和C_(min)加值变化不显著(p>0．05)。偏相关性分析显示，植株的磷吸收V_(max)、K_m和C_(min)值与体内磷浓度显著相关(P<0．01、P<0．05、P<0．05)，而与供磷水平之间无显著的相关性(P>0．05)。这些结果表明植株的磷吸收状态与体内磷浓度具有密切的关系。
在含1000μM KH_2PO_4的营养液中培养23天后，Qi319植株转入无磷营养液中继续培养10天，观察缺磷胁迫期间植株的体内磷浓度和磷吸收的变化。结果显示，随缺磷胁迫时间的延长，植株的体内磷浓度逐渐降低，而磷吸收V_(max)和对Pi的亲和力则逐渐增大。相关性分析表明在缺磷胁迫期间植株的磷吸收V_(max)、K_m和C_(min)值与茎叶及根部磷浓度之间也存在显著相关性(P<0．01)。
对在无磷营养液中生长的玉米植株进行叶面供磷处理3天，发现植株的体内磷浓度逐渐升高，且茎叶与根部磷浓度存在较大差异。当茎叶磷浓度已达足磷水平时，根部磷浓度虽有所增加，但仍处在严重缺磷状态，而此时植株的根系磷吸收表观V_(max)值和对Pi的亲和力显著减小(P<0．01)。上述结果表明，叶面供磷处理植株的根系磷吸收与茎叶磷浓度有关，这为系统磷信号调控根系磷吸收的观点提供了新证据。
2．依据茎叶磷浓度估测植株的磷吸收状态
玉米植株磷吸收动力学参数与体内磷浓度之间存在着显著的相关性，预示着可依据体内磷浓度来估测玉米植株的磷吸收状态。本研究对玉米植株的磷吸收动力学参数(V_(max)、K_m和C_(min))与茎叶磷浓度进行线性回归分析，得到三个具有较高拟合优度(R~2)的线性方程式。利用这三个方程式，依据茎叶磷浓度估算不同磷处理植株的磷吸收动力学参数，并与传统的离子耗竭法测定的参数值相比较。结果显示，除缺磷预处理植株在恢复供磷后的几天内，V_(max)的估算值比离子耗竭技术的测定值偏低外，不同磷处理植株的磷吸收动力学参数(V_(max)、K_m和C_(min))的估算值均与离子耗竭法的测定值相吻合。以上结果表明，玉米茎叶磷浓度可反映根系的磷吸收状态，因此，依据茎叶磷浓度估算根系磷吸收动力学参数可成为一个方便快捷的估测玉米植株磷吸收状态的新方法，该方法对指导玉米精准化施用磷肥和玉米高产有一定意义。
二、低磷胁迫对玉米成熟叶磷转运的影响
用含1000μM KH_2PO_4营养液培养23天的Qi319植株移入低磷(0．1μM Pi)营养液后(0-14天)，检测茎基部和成熟叶叶片木质部伤流液的Pi浓度，以及成熟叶叶片韧皮部渗出液的磷含量，来反映成熟叶的磷输入和输出的变化。结果显示，在低磷条件下，通过木质部向成熟叶输入的磷明显减少，通过韧皮部输出的磷则相对增多。
用成熟叶制备质膜囊泡进行磷吸收测定，发现来自于低磷处理植株质膜囊泡的磷吸收表观V_(max)值，与来自高磷对照植株的相比显著增大(P<0．01)，表明成熟叶的细胞磷吸收能力在低磷胁迫下明显增强。为探究该动力学特征变化的生理意义，在成熟叶的叶片上局部施加含NEM(跨质膜磷转运抑制剂)或不含NEM的~(32)P标记Pi溶液，检测叶片(去除Pi施用区域)和叶片韧皮部渗出液的放射活度，结果显示，在NEM存在时，叶细胞从质外体中吸收~(32)P标记Pi的量显著减少(P<0．01)，叶片韧皮部渗出液的放射活度也显著降低(P<0．01)，这表明叶细胞从质外体中吸收Pi与叶的磷输出有关。玉米成熟叶的细胞在低磷胁迫下增强磷吸收能力，可能有利于从低Pi浓度的质外体及木质部中吸收较多的Pi，这对维持细胞的正常生理活动和增加叶的磷输出具有一定的意义。
三、生长素和细胞分裂素在低磷诱导的根系构型改变中的作用
植物根系的胚后发育是高度可塑的，植物通常通过调控根系的胚后发育和修饰根系构型以更好地适应外部环境。在自然生态系统中，有效磷不足是限制植物生长的重要因素之一，而植物对磷养分的吸收能力与根系构型密切相关。植物激素，如生长素和细胞分裂素都参与根系的胚后发育调控和构型修饰，但这两种激素及其之间的互作在低磷诱导的根系构型改变中的作用目前仍了解甚少。
自交系99037是通过细胞工程技术获得的、来自于Qi319的耐低磷细胞突变体。在不同供磷条件下，99037植株较Qi319有更长的轴根(基根和不定根)和侧根以及更高的磷吸收累积能力；在田间99037植株也比Qi319具有更高的干物质和籽粒产量。
将99037和Qi319植株在高磷(1000μM Pi)或低磷(5μM Pi)营养液中培养18天，观察低磷胁迫下根系IAA和玉米素水平与分布及根系构型的变化。结果显示，在低磷条件下，玉米素浓度在植株的轴根幼嫩区段(约1 cm)和成熟区段(去除轴根幼嫩区段)以不同的幅度显著降低(P<0．05)，IAA浓度及其与玉米素浓度的比值在轴根幼嫩区段明显增大，在轴根成熟区段却显著减小(P<0．05)；同时在低磷条件下，植株的轴根数目、侧根平均长度和密度比在高磷条件下显著减少(P<0．05)，而轴根平均长度却显著增加(P<0．05)，因而形成了轴根长的根系。上述结果提示，在低磷条件下，玉米植株根系的构型发生改变，与生长素和玉米素在根部的水平和分布以及两种激素浓度比例的变化有关。
为进一步验证，本工作用6-BA和NAA单独或组合处理以及用生长素极性运输抑制剂(TIBA)处理不同供磷条件下生长的两个自交系植株，观察根系结构的变化。结果支持了上述推测。
99037和Qi319植株在根系结构、根系IAA浓度和分布、IAA与玉米素浓度比例、以及其侧根对低磷胁迫和TIBA的敏感性等方面存在差异，这些差异及差异间的对应关系也支持上述推测。
基于以上结果可以认为，在低磷条件下，生长素和细胞分裂素在玉米根系中的浓度和分布及两种激素的浓度比例发生明显的变化，这些变化以及两种激素间的互作在低磷诱导的根系构型改变中起着重要作用。寻找玉米磷信号和激素信号网络的共有接点无疑会加深对玉米耐低磷机制的认识。
As an essential macronutrient for plant growth and development, phosphorus (P) not only is an important architectural component of plant cells, but also plays an important role in cell metabolism and signal transduction. However, low availability of phosphate (Pi) in soil has become a major constraint for plant growth and production, due to its low immobility. To adapt the low-P conditions, plants have evolved complex strategies including modifications of root architecture, improvement of Pi acquisition and recycling etc. In recent years, some progress has been made in the studies on regulation of Pi uptake in plants. Nonetheless, the relationship between Pi uptake and internal P concentrations (IPCs) of plants needs to be further explored; kinetic characteristics of Pi uptake by cells of mature leaf under low P stress and its physiological significance remain to be discovered; and knowledge concerning the role of phytohormones in low-P response of plants remain to be elucidated. In the present work, using maize (Zea mays L.) inbred line Qi319, the relationship between Pi uptake and IPCs of plants was analyzed, changes of kinetic characteristics of Pi uptake by cells of mature leaf under P deficiency were studied, and the physiological role of these changes in leaf P output was discussed. Furthermore, root architectural characteristics, levels and distribution of endogenous auxin and cytokinkin within root system, and effect of exogenous phytohormones and chemical inhibitor on root architecture were investigated in seedlings of Qi319 and 99037 (a low P-tolerant line derived from Qi319) under different P conditions. The objective of the present study is to reveal regulation mechanisms of Pi uptake and transport, and the role of auxin and cytokinnin in the low-P-induced alterations of root architecture in maize.
1. Regulation of Pi uptake by maize roots
(1) Relationship between Pi uptake and internal P concentrations of plants
Seedlings of maize imbed line Qi319 were grown under different P supplies (0.1-1,000μM KH_2PO_4) for 25 days, and the relationship among P supply level, IPCs, and Pi uptake of plants were investigated. The results indicated that IPCs of the plants increased with the elevation of P supply level, whereas Pi uptake rate (V_(max)) and affinity for Pi of the plants reduced. Correlation analysis showed that apparent V_(max) value of Pi uptake was reversely related to external P concentrations (EPCs), shoot and root P concentrations (SPCs and RPCs) of the plants within the entire P supply range (0.1-1,000μM) (P < 0.01). Among the P supply range from75μM to 1,000μM apparent K_m and C_(min) values of Pi uptake were positively related to EPCs. SPCs and RPCs respectively (P < 0.01). As P supply level ranged from 0.1μM to 75μM, there was no significant changes in K_m or C_(min) values. Partial correlation analysis revealed that these parameters (V_(max), K_m and C_(min)) were only significantly correlated with SPCs and RPCs (P < 0.05), not EPCs (P > 0.05). Taken together, these results showed that Pi uptake by roots had a close relationship with the IPCs.
Qi319 seedlings grown in nutrient solution containing 1,000μM KH_2PO_4 for 23 days were deprived of Pi for 10 days, and variations of IPCs and Pi uptake during P deprivation were investigated. The results indicated that SPCs and RPCs gradually decreased with the prolongation of P deprivation period, while affinity for Pi and Pi uptake rate (V_(max)) of the plants increased continually. Furthermore, significant correlations were also clearly showed between the parameters (V_(max), K_m and C_(min)) and IPCs of shoots and roots in the phase of P deprivation (P < 0.01).
Seedlings of Qi319 grown in nutrient solution without P were supplied with Pi through leaves. It was observed that within 3 days of the P recovery period, IPCs of the plants increased gradually. However, difference in IPCs between the shoots and roots was considerable: the SPCs had increased to a sufficient P level, while the RPCs, though increased at some extent, were still under severe P deficiency. Meanwhile, both Pi uptake capacity (V_(max) and affinity for Pi of roots in these seedlings decreased significantly compared to those without P supply (P < 0.01). These results showed that the Pi uptake status of roots have a relationship with SPCs of the plants in this P recovery period, and provided compelling evidence for the hypothesis that systemic P signal regulates Pi uptake of roots.
(2) Estimation of Pi uptake status according to SPCs of maize plants
Significant correlation between IPCs and parameters of Pi uptake kinetics suggested that Pi uptake by maize plants could be estimated by IPCs. In the present study, three equations with high determinants of coefficient (R~2) were obtained based on the linear regressions of the kinetic parameters and SPCs. With these equations, values of K_m, C_(min) and V_(max) of Pi uptake by seedlings grown in different circumstances were calculated by SPCs and compared with the values determined by Pi depletion technique. For V_(max), there was a parallel relationship between the values estimated by SPCs and determined by Pi depletion technique, only except the period of resupplying Pi to the Pi-starved seedlings over several days. For K_m and C_(min). the values estimated by SPCs were consistent with those obtained from Pi depletion experiments. These results indicated that SPCs basically reflect the status of Pi uptake of plants in a linear manner, and it is possible to estimate the Pi uptake kinetic parameters according to SPCs, which is potential to be a novel and convenient method for estimating the Pi-uptake status of maize plants. This method would be helpful for applying P fertilizers finely and economically and achieving high yield of maize.
2 Effect of low-P stress on P transport in maize mature leaf
(1) After grown under 1000μM KH_2PO_4 for 23 days, Qi319 seedlings were treated under low P (0.1μM Pi) condition (0-14 days), and Pi concentrations of stem and mature leaf xylem saps as well as P contents of mature leaf phloem exudates were monitored. The results indicated that P which was imported to mature leaf through xylem decreased, whereas P output of the leaf through phloem was enhanced relatively under low-P conditions.
(2) Pi uptake assay with plasma membrane vesicles revealed that apparent V_(max) value of Pi uptake by plasma membrane vesicles which were prepared from the mature leaves of seedlings treated under low P condition was greater than those of the control plants (P < 0.01). The result indicated that Pi uptake by cells of mature leaf was enhanced under P deficiency. To explore the physiological significance of variations of Pi uptake by cells of mature leaf under P deficiency, the maize mature leaf was applied locally with Pi solutions labeled by ~(32)P in the presence or absence of an inhibitory agent (NEM) for Pi transport across plasma membranes; and then, radioactivity of the leaf (laminas where ~(32)P was applied were cut out) and leaf phloem exudates were measured. The results indicated that in the presence of NEM, ~(32)P labeled Pi uptake by the leaf cells from leaf apoplasts was inhibited significantly (P< 0.01), and synchronously, radioactivity of the leaf phloem exudates decrease significantly compared with that in the absence of NEM (P < 0.05). showing a relationship between Pi uptake by leaf cells from apoplasts and P export of the leaf. Taken together, it could be concluded that under low-P stress capacity of Pi uptake by cells of mature leaf was enhanced, which would benefit leaf cells to absorb Pi from leaf apoplasts (including xylem apoplasts), and maintain the normal physiological activity of the cells and increase the P export of mature leaf.
3 Roles of auxin and cytokinin in the low-P-induced alterations of root architecture
The postembryonic developmental program of plant root system is plastic, allowing changes in root architecture to adapt to environmental conditions including P availability. Insufficient of available Pi in soil is one of the important factors that strongly limit plant growth. Root architecture, to some extent, determines the capacity of plant Pi acquisition. Phytohormones, such as auxin and cytokinin, involve in the postembryonic development of root system, however, the roles of both hormornes and their mutual interaction in the low-P-induced alterations of root architecture have been unclear so far.
The inbred line 99037 is developed from Qi319 by cellular engineering. Under different P supply levels, 99037 plants have longer lateral and axile roots (including primary and adventitious roots) and higher capacity of P uptake and accumulation than Qi319. In the field experiments, both total dry weight and seed yield of 99037 are greater than those of Qi319, respectively.
Seedlings of 99037 and Qi319 were grown hydroponically under low (LP, 5μM Pi) or high (HP, 1,000μM Pi) P conditions for18 days, and the root architecture and levels and distribution of IAA and zeatin within root system were investigated. The results showed that under LP, zeatin concentrations in both young segments of axile roots (1 cm long from apex, YSARs) and mature segments of axile roots (behind YSARs) decreased (P < 0.05) compared to those under HP; IAA concentrations and the ratio of IAA to zeatin (IAA concentrations/zeatin concentrations) increased markedly in YSARs under LP, while reduced significantly in MSARs (P < 0.05), compared to those under HP. Synchronously, the number of aixle roots, and the density and average length of lateral roots decreased significantly (P < 0.05), whereas average length of axile roots increased significantly (P < 0.05) under LP, compared to those under HP. These results indicated that root architecture, levels and distribution of auxin and zeatin as well as the ratio of IAA to zeatin within root system were altered notably under LP, implying that variations of levels and distribution of IAA and zeatin as well as their mutual interaction within root system played roles in the low-P-induced alterations of root architecture.
To validate this presumption, seedlings of both lines grown under LP or HP were treated with 6-BA and NAA solely or together, or an auxin porlar transport inhibitor (TIBA), and the alterations of root architecture of the plants were investigated. The results supported the presumption that variations of levels and distribution of auxin and cytokinin as well as interaction between them within root system played roles in alterations of root architecture under low-P conditions. In addition, this presumption was further supported by the differences in root architecture, level and distribution of IAA, ratio of IAA to zeatin, and the resistence of lateral roots to low-P stress and TIBA between 99037 and Qi319 root systems.
In summary, levels and distribution of auxin and cytokinin as well as the ratio of both within root system vary notably under LP condition. And these variations and interaction between the two hormones play an important role in the low-P-induced alterations of maize root architecture. Seeking the cross-talk of phytohormone and phosphorus signaling network may help to understand the low P tolerance mechanism in maize.
引文
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