Low-P tolerance by maize (Zea mays L.) genotypes: Significance of root growth,and organic acids and acid phosphatase root exudation

We investigated some mechanisms, which allow maize genotypes to adapt to soils which are low in available P. Dry matter production, root/shoot-ratio, root length and root exudation of organic acids and acid phosphatase were investigated in four maize genotypes grown under P-deficient and P-sufficient conditions in sterile hydroponic culture. A low-P tolerant, an acid-tolerant and a low-P susceptible genotype of maize were compared with a Swiss commercial cultivar. The study found increased root development and increased exudation of acid phosphatase under P-deficient conditions in all maize genotypes, except for the Swiss cultivar. Effects on root formation and acid phosphatase were greater for the low-P tolerant than for the low-P susceptible, and the acid soil tolerant genotypes. Organic acid contents in root tissues were increased under P deficiency and related to increased PEPC activity. However, the increase in contents was associated with an increase in exudation for the low-P tolerant genotype only. The low-P susceptible genotype was characterized by high organic acid content in roots and low organic acid exudation. The organic acids content in the phloem exudates of shoots was related to root exudation under different P supply, to the difference between lines in organic acids root content, but not to the low-P tolerance or susceptibility of maize genotypes.     

缺磷白羽扇豆排根与非排根区根尖分泌有机酸的比较

采用根系分泌有机酸原位收集方法及高效液相色谱技术分析了供磷及缺磷后不同时间白羽扇豆(LupinusalbusL .)非排根区根尖和排根分泌有机酸的种类和数量 ,以及相应的根尖、排根组织 ,茎木质部、韧皮部汁液中有机酸含量的变化。结果表明 :(1)缺磷能够诱导白羽扇豆根系产生大量排根 ,根系的有机酸分泌量也明显增加。 (2 )无论在供磷或缺磷条件下 ,排根与非排根区根尖组织中的有机酸种类相同 ,但排根主要分泌柠檬酸和苹果酸 ,而非排根区根尖主要分泌苹果酸和乙酸。 (3)缺磷后非排根区根尖分泌苹果酸的量增加 ,至第 17天达到高峰 ;排根开始分泌柠檬酸的时间相对较晚。缺磷后排根分泌柠檬酸的量随缺磷时间的延长不断增加。 (4 )在缺磷的排根与非排根区根尖组织和茎木质部伤流液中含有大量柠檬酸和苹果酸 ,但在茎韧皮部汁液中则几乎检测不到这两种有机酸。上述结果表明 ,尽管排根和非排根区根尖组织中的有机酸种类相同 ,但它们向外分泌的有机酸种类不同。缺磷后排根及非排根区根尖增加向外分泌的有机酸主要在根中合成     

Root cell-wall properties are proposed to contribute to phosphorus (P) mobilization by groundnut and pigeonpea

Groundnuts showed a superior ability to take up phosphorus (P) from two soils of extremely low fertility, where sorghum and soybean died of P deficiency. This ability could not be attributed to differences in root development, to P uptake parameters such as C_min, or to the excretion of root exudates capable of solubilizing iron- (Fe-P) and aluminum-bound P (Al-P), the sparingly soluble P forms in soils. A new P solubilizing mechanism (called `contact reaction') which occurs at the interface between root surface and soil particles, is therefore proposed. Isolated cell walls from groundnut roots solubilized more P from P-fixing minerals than those from sorghum and soybean roots. The P-solubilizing activity of groundnut root cell-walls might therefore be related to the superior growth of this crop under P-deficient conditions. The P-solubilizing active sites in groundnut root cell walls were located at the root surface and could act as chelating agent with Fe(III). This P-solubilizing active component in the cell walls could be extracted by NaOH, but not by HCl, and was identified as a small molecule through column chromatography with Sephadex LH-20. The P-solubilizing ability of pigeonpea root cell-walls was examined and found to be as high as that of groundnut. As pigeonpea plants excrete significant amount of root exudates with Fe-P solubilizing ability only after they flower, the P-solubilizing ability of root cell-walls may partially explain the high P efficiency of this species before it flowers.     

Aluminum resistance in two cultivars of Zea mays L.: Root exudation of organic acids and influence of phosphorus nutrition

Root exudation of organic acids as Al-chelating compounds and P nutrition have been suggested to play a major role in Al-resistance in higher plants. Effects of Al exposure on maize plant growth, and organic acid root content and root exudation under various levels of P nutrition were examined. Sikuani, a Colombian maize cultivar tolerant to acid soils with high Al saturation, and Corso, a Swiss cultivar, were grown in sterile hydroponic conditions for 21 days. Al-caused inhibition of root growth was lower in Sikuani than in Corso. Al effect on plant growth was decreased with increasing P content in roots. Al content in roots increased with increasing P content and was higher in Sikuani than in Corso. When exposed to Al, the contents in root apices as well as the root exudation of citric and malic acids in Corso and citric, malic and succinic acids in Sikuani increased, and were higher in Sikuani than in Corso. Increased PEP carboxylase (PEPC) activity in root apices after Al exposure partially explained the variations of organic acid content in the roots. These Al-induced changes in PEPC activity, organic acid content and exudation were reduced in plants supplied with higher P concentrations during the 21 days prior to treatment. Increased secretion of organic acids after exposure to Al appeared to be specific to Al and was not totally explained by increased root content in organic acids.     

Citrate, Malate, and Succinate Concentration in Exudates from P-Sufficient and P-Stressed Medicago sativa L. Seedlings

Under certain stress conditions roots exude organic molecules, which may facilitate the uptake of nutrients. The objective of this research was to identify and measure the effect of low P upon the exudation of organic acids by roots of alfalfa (Medicago sativa L.) seedlings. Surface-sterilized alfalfa seeds were grown aseptically in sterile sand using an apparatus specially designed for the addition of ±P nutrient solutions and for the collection of root exudates. Citric, malic, and succinic acids were detected in the root exudates of 24-day-old alfalfa seedlings. Citrate exudation from the roots of P-stressed alfalfa was 182% that of plants receiving a complete nutrient solution. The increased release of citrate may provide a mechanism by which P-stressed plants enhance the availability of P in the rhizosphere.     

有机酸对土壤无机态磷转化和速效磷的影响

土壤有效磷含量低是影响作物生产的重要限制因素之一.作物根分泌活化难溶性磷的有机酸对改善其磷素营养具有重要意义.采用张守敬和Jackson无机磷分级方法,以湖北省3种pH值土壤为材料,加入不同磷源和有机酸,经过室温培养后,测定速效磷含量和无机磷组分的变化.结果表明:施磷显著提高了土壤中速效磷含量,中性土、酸性土Fe-P和Al-P含量大幅上升, Fe-P占增加量的50%以上,而碱性土Ca-P含量显著增加.加施有机酸使中性土速效磷含量增多,除苹果酸处理的变幅较小外,草酸和柠檬酸的加入速效磷显著增加.由于有机酸的作用,中性土Al-P含量下降,Ca-P含量上升,变幅大小依次为草酸＞柠檬酸＞苹果酸;酸性土中Al-P含量呈下降趋势,碱性土中Ca-P含量有不同程度的减少,3种土壤中O-P含量均有所增加.说明有机酸活化的磷主要来源于中性土和酸性土Al-P、Fe-P及碱性土Ca-P中的磷,同时有机酸能够促进土壤中闭蓄态磷(O-P)的形成与积累.     

子叶磷在白羽扇豆缺磷适应性反应中的作用

实验用液体培养的方法,对比分析了在不同供磷条件下,白羽扇豆子叶中的磷对植物生长发育的影响,以及排根和根尖中有机酸积累和分泌的作用,结果表明,子叶中的磷能使白羽扇豆在完全缺磷２３d的环境中,不仅没有使干物质的积累减少,反而使干物质的积累略有增加,相反,如果没有子叶磷的供给,则使白羽扇豆在缺磷环境中产生强烈的抗胁迫反应,表现在干物质的积累明显下降,根系能产生大量的排根,排根能积累和分泌大量的柠檬酸,而根尖能积累和分泌萍果酸,在整个缺磷反应过程中,根尖中苹果酸的分泌要早于排根可柠檬酸的积累和分泌。     

Root excretion of carboxylic acids and protons in phosphorus-deficient plants

Phosphorus deficiency-induced metabolic changes related to exudation of carboxylic acids and protons were compared in roots of wheat (Triticum aestivum L. cv Haro), tomato (Lycopersicon esculentum L., cv. Moneymaker), chickpea (Cicer arietinum) and white lupin (Lupinus albus L. cv. Amiga), grown in a hydroponic culture system. P deficiency strongly increased the net release of protons from roots of tomato, chickpea and white lupin, but only small effects were observed in wheat. Release of protons coincided with increased exudation of carboxylic acids in roots of chickpea and white lupin, but not in those of tomato and wheat. P deficiency-induced exudation of carboxylic acids in chickpea and white lupin was associated with a larger increase of carboxylic acid concentrations in the roots and lower accumulation of carboxylates in the shoot tissue compared to that in wheat and tomato. - Citric acid was one of the major organic acids accumulated in the roots of all investigated species in response to P deficiency, and this was associated with increased activity and enzyme protein levels of PEP carboxylase, which is required for biosynthesis of citrate. Accumulation of citric acid was most pronounced in the roots of P-deficient white lupin, chickpea and tomato. Increased PEP carboxylase activity in the roots of these plants coincided with decreased activity of aconitase, which is involved in the breakdown of citric acid in the TCA cycle. In the roots of P-deficient wheat plants, however, the activities of both PEP carboxylase and aconitase were enhanced, which was associated with little accumulation of citric acid. The results suggest that P deficiency-induced exudation of carboxylic acids depends on the ability to accumulate carboxylic acids in the root tissue, which in turn is determined by biosynthesis, degradation and partitioning of carboxylic acids or related precursors between roots and shoot. In some plant species such as white lupin, there are indications for a specific transport mechanism (anion channel), involved in root exudation of extraordinary high amounts of citric acid. This revised version was published online in June 2006 with corrections to the Cover Date.     

Effects of low pH and aluminum stresses on common beans (Phaseolus vulgaris) differing in low-phosphorus and photoperiod responses

Using common beans differing greatly in the response to photoperiod and low-phosphorus (P) stress, we investigated their responses to acidity and aluminum (Al)toxicity and the relationship between Al tolerance and organic acid exudation under Al or low P stress. A genotype Ginshi was found to be sensitive to low pH treatment. When exposed to pH 4.5, serious curvature in the root tips of cv. Ginshi was observed; however, it was completely corrected by the application of 5 or 10 μmol/L AlCl3; increasing calcium (Ca) could ameliorate Al toxicity, but it could not correct root curvature at pH 4.5. Common beans showed significant differences in both root growth and Al tolerance, and the varieties from the Andes were more tolerant to Al toxicity than those from the Mesoamerican origin. In the presence of 50 μmol/L AlCl3,all the common bean genotypes exuded citrate, and a significant difference in the amounts of citrate was observed among genotypes. The genotypes originated in the Mesoamerica tended to release more citrate than other origins in the presence of Al. The P-inefficient genotype DOR364 exuded more citrate than the P-efficient genotype G19833 in the presence of 50 μmol/L AlCl3, whereas no organic acids were detected in root exudates under low-P stress. A reduction of citrate exudation in the DOR364, but a slight increase of citrate exudation in the G19833, was observed under Al stress after they were exposed to 6-d P starvation. These results suggest that different low-P or Al tolerance in common beans might not be associated with organic acid exudation.     

稻、麦根系H~ 的分泌与介质磷水平的关系

水稻、小麦根系H~ 的分泌量随供磷水平的降低而增加,并存在明显的昼夜变化。在自然光照下H~ 分泌量随光强度增加而增多,同时强光比黑暗时H~ 分泌对磷供应水平更为敏感。磷供应不足还诱导水稻根系柠檬酸分泌量增加,而苹果酸则差异不明显。难溶性磷的溶解率与根系H~ 和柠檬酸分泌所导致的根际pH下降有密切联系。因此,在有效磷不足的条件下可明显提高稻、麦根际土壤中难溶性磷的利用率,其中丰产型小麦和粳稻品种对土壤中磷利用的根际效应更为显著。     

Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.)

White lupin was grown in a quartz sand–soil mix with poorly available Ca phosphate. The plants were harvested on days 21, 35 and 51 and DNA was extracted from the non-cluster roots, the young, mature and senescent cluster roots with adhering soil. Bacterial community structure was examined by PCR-DGGE of 16S rDNA, digitisation of the band patterns and multivariate analyses. In all root zones the bacterial community structure changed with plant age. The communities in the rhizosphere of the non-cluster roots were always different from those of the cluster roots. The bacterial communities of the cluster roots were cluster age and plant age dependent. The differences in bacterial community structure between the cluster root age classes were significant on days 35 and day 51 but not on d 21. A separate experiment, in which root exudates and samples for PCR-DGGE were collected simultaneously, showed that both bacterial and eukaryotic (18S rDNA) community structures change with organic acid exudation. While eukaryotic community structure of the cluster roots was correlated with citric acid exudation, bacterial community structure was correlated with cis-acconitic, citric and malic acid exudation.     

秋茄(Kandelia candel (L))根系分泌低分子量有机酸及其对重金属生物有效性的影响

应用电感耦合等离子体质谱(ICP-Ms)与高效液相色谱(HPLC)分别对福建漳江口红树林湿地不同土壤结构(砂质与泥质)根际与非根际沉积物中重金属(Cu,Pb,Cd,Zn)含量,以及生长于砂质与泥质滩涂上的红树植物秋茄(Kandelia candel(L)Druce))幼苗根系分泌物中的低分子量有机酸进行测定。在室内模拟秋茄根系分泌的低分子量有机酸,作为重金属提取剂提取沉积物中可溶解态与碳酸盐结合态重金属,并与欧盟标准物质局(BCR)连续提取法相比较,探讨红树根系分泌的低分子量有机酸对红树林沉积物重金属生物有效性的影响。研究结果表明:漳江口红树林泥质沉积物中重金属含量大于砂质沉积物,根际沉积物大于非根际沉积物。两样地沉积物中重金属的赋存形态主要以铁锰氧化物结合态为主,根际沉积物中可交换态与碳酸盐结合态重金属含量均大于非根际沉积物。秋茄根系分泌低分子量有机酸为甲酸,丁酸,苹果酸,柠檬酸,乳酸。不同土壤结构对秋茄根系分泌的苹果酸,柠檬酸,乳酸有显著影响(P<0.05)。以低分子量有机酸作为提取剂对沉积物中可溶解态与碳酸盐结合态重金属的提取率表现为:柠檬酸>混合酸>苹果酸>乳酸>乙酸,低分子量有机酸对红树林沉积物重金属的生物有效性有促进作用。     

Quantitative evaluation of the role of organic acid exudation in the mobilization of rock phosphate by rape

Phosphorus-deficient rape plants appear to acidify part of their rhizosphere by exuding malic and citric acid. A simulation model was used to evaluate the effect of measured exudation rates on phosphate uptake from Mali rock phosphate. The model used was one on nutrient uptake, extended to include both the effect of ion uptake and exudation on rhizosphere pH and the effect of rhizosphere pH on the solubilization of rock phosphate. Only the youngest zones of the root system were assumed to exude organic acids. The transport of protons released by organic acids was described by mass flow and diffusion. An experimentally determined relation was used describing pH and phosphate concentration in the soil solution as a function of total soil acid concentration. Model parameters were determined in experiments on organic acid exudation and on the uptake of phosphate by rape from a mixture of quartz sand and rock phosphate. Results based on simulation calculations indicated that the exudation rates measured in rape plants deficient in phosphorus can provide the roots with more phosphate than is actually taken up. Presence of root hairs enhanced the effect of organic acid exudation on calculated phosphate uptake. However, increase of root hair length without exudation as an alternative strategy to increase phosphate uptake from rock phosphate appeared to be less effective than exudation of organic acids. It was concluded that organic acid exudation is a highly effective strategy to increase phosphate uptake from rock phosphate, and that it unlikely that other rhizosphere processes play an important role in rock phosphate mobilization by rape.     

异质低磷胁迫下马尾松家系根构型和磷效率的遗传变异

以7个马尾松(Pinus massoniana)一代种子园自由授粉家系为材料, 设置同质低磷(P)胁迫和异质低P胁迫模拟的盆栽试验, 系统研究马尾松家系对不同类型低P胁迫的适应机制和P效率变异规律。结果表明, 参试马尾松家系的苗高、地径和生物量等P效率指标均表现出显著的家系变异, 主要P效率指标的家系遗传力均较高, 干物质积累量的广义遗传力大于0.80, 揭示了马尾松P营养效率的较大遗传改良潜力。马尾松对不同类型低P胁迫的适应机制有所差异。在同质低P胁迫下, ‘3201’、‘1217’等高P效率家系的根系主要参数均高于低P效率家系, 表明整体根系参数的适应性变化是P效率和生物量形成的决定因素。在异质低P胁迫下, 高P效率马尾松家系在表层富P介质的根系分布量、分布比例均显著增加, 表层根系参数与马尾松家系P效率呈显著正相关, 揭示根系空间构型的适应性变化是决定马尾松高P效率的重要生物学基础。表层根系生物量、表层根相对比例的家系遗传力达0.88和0.72, 证实了以马尾松根构型的适应变化为突破口, 选育具有理想根构型和较高P效率的马尾松家系。     

Identification of aliphatic and aromatic acids in root and seed exudates of peas,cotton, and barley

Summary We detected aromatic and aliphatic acids in root and seed exudates of aseptic cultures of pea, cotton and barley plants by thin-layer and gas-liquid chromatography. There were traces of p-hydroxybenzoic acid in the root and seed exudates of all three plant species. Acid hydrolysis of pea and barley seed exudates yielded p-hydroxybenzoic, and of cotton seed exudates yielded p-coumaric acid, as the predominant aromatic acid constituents of materials exuded by the germinating seeds. Lactic was the predominant aliphatic acid detected in pea and barley root exudates whereas malic acid was predominant in cotton exudates. With the exception of citric acid in peas, malic acid was the predominant acid found in pea, cotton and barley seed exudates. The germinating seed was responsible for a large portion of the total aliphatic and aromatic acid exudation of the seedling plant grown aseptically for 14 days. Trade names are used in this publication only to provide scientific information. Their use does not constitute a guarantee of the products named and does not signify that they are approved by the U.S. Department of Agriculture to the exclusion of others of suitable composition.     

The role of cell wall components from groundnut roots in solubilizing sparingly soluble phosphorus in low fertility soils

Groundnuts have a superior ability to take up P from soils with low P fertility compared to sorghum and soybean. Previous experiments showed that this ability was neither attributable to better root development nor to root exudates capable of solubilizing Fe- and Al-bound P, the sparingly soluble P forms in soils. Direct "contact reactions" between cell wall components from these 3 plant species (groundnut, soybean and sorghum) and P-fixing Fe and Al minerals were examined. Cell wall preparations from groundnut roots showed a superior P solubilizing ability than those of soybean and sorghum. Cell wall activity of groundnut roots may thus at least partly explain the superior growth of this crop under P-deficient conditions. To characterize the active site responsible for P solubilization, effects of pH, heat, addition of cations, and digestion with enzymes (pectinase and cellulase) or HCl on P solubilization were investigated. Conclusion are 1) Solubilizing ability is not related to root CEC because soybean with higher root CEC showed an inferior solubilizing ability compared to groundnut. 2) The reaction site of cell-walls of groundnut roots is stable against heating and digestion with cellulase and pectinase. 3) Solubilizing ability was severely reduced by digestion with HCl. 4) Pre-treating cell walls with either Al3+, Fe3+, or Ga3+ decreased solubilizing ability but cations with lower valency such as Na+, K+, Ca2+ or Mg2+ had no effect. Soaking roots of groundnuts grown in solution culture in 0.5 M NaOH for 30 seconds prior to cell wall preparation led to a 30% reduction in solubilization of P from FePO4 without permanently damaging plants. This suggests that 5) the active component of the cell walls was located on the root epidermal cell surfaces. Based on these results a phosphorus solubilizing mechanism is proposed.     

一株红壤溶磷菌的分离、鉴定及溶磷特性

【目的】为了提高红壤磷素利用率,探讨溶磷菌溶磷机理。【方法】利用难溶性无机盐培养基从花生根际土壤样品中分离到一株溶磷菌C5-A,结合菌落形态特征、生理生化和16S rRNA序列确定该菌株的系统发育地位;通过菌株C5-A在NBRIP液体培养基培养过程中培养液pH变化确定其溶磷能力;利用液体发酵实验测定不同的碳源、氮源对菌株C5-A溶磷的影响;通过高效液相色谱检测C5-A在不同氮源培养液中有机酸的种类和浓度。【结果】菌株C5-A鉴定为洋葱伯克霍尔德氏菌(Burkholderia cepacia),遗传稳定性较好。在FePO4和AlPO4培养液中,菌株C5-A的溶磷量和pH变化呈显著负相关;菌株C5-A对磷酸三钙、磷酸铝、磷酸铁、磷矿粉均有较强的溶解能力,最高溶磷量分别为125.79、227.34、60.02和321.15 mg/L;菌株C5-A对不同浓度的两种磷矿粉有较强的溶解能力;分别以麦芽糖和草酸铵为碳源和氮源时溶磷量最高。高效液相色谱检测出10种有机酸,分别为草酸(葡萄糖酸)、乙酸、苹果酸、琥珀酸和5种未知有机酸,然而,乙酸而非草酸似乎是影响C5-A溶磷的重要有机酸。【结论】从红壤花生根际土壤中筛选到一株对难溶性无机盐具有较强溶解能力溶的菌株C5-A,有望为开发高效红壤微生物磷肥提供种质资源。     

Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic acids

The nature and quantity of low-molecular organic acids (LOAs) exuded by the roots of nine species of calcifuge and nine species of acidifuge wild plants from northern Europe were determined by ion chromatography. Particular attention was paid to differences between the calcifuge and the acidifuge species in the proportions of different LOAs in their root exudates. Great differences in mol% root exudation between the calcifuge and the acidifuge species were found in some acids. The calcifuge species exuded more acetic acid, the acidifuge species more oxalic acid and much more citric acid. In three calcifuge species, however, root exudation of oxalic acid was appreciable, whereas acetic acid exudation was low in these species. The phosphate- and Fe-solubilizing ability of eight LOAs in a rhizosphere limestone soil was also tested. Oxalic acid was the most efficient phosphate solubilizer and citric acid, by far, the most efficient Fe-solubilizer at the concentration (10 mM) tested. It might be hypothesized that acidifuge species use oxalate to solubilize phosphate and citrate to solubilize Fe, in limestone soil. The inability of calcifuge species to grow in limestone soil might, therefore, be due to low root exudation of these acids and, as a result, inability to solubilize phosphate and Fe in limestone soil.     

Root carboxylate exudation capacity under phosphorus stress does not improve grain yield in green gram

Key message

Genetic variability in carboxylate exudation capacity along with improved root traits was a key mechanism for P-efficient green gram genotype to cope with P-stress but it did not increase grain yield.

Abstract

This study evaluates genotypic variability in green gram for total root carbon exudation under low phosphorus (P) using ¹⁴C and its relationship with root exuded carboxylates, growth and yield potential in contrasting genotypes. Forty-four genotypes grown hydroponically with low (2 μM) and sufficient (100 μM) P concentrations were exposed to ¹⁴CO₂ to screen for total root carbon exudation. Contrasting genotypes were employed to study carboxylate exudation and their performance in soil at two P levels. Based on relative ¹⁴C exudation and biomass, genotypes were categorized. Carboxylic acids were measured in exudates and root apices of contrasting genotypes belonging to efficient and inefficient categories. Oxalic and citric acids were released into the medium under low-P. PDM-139 (efficient) was highly efficient in carboxylate exudation as compared to ML-818 (inefficient). In low soil P, the reduction in biomass was higher in ML-818 as compared to PDM-139. Total leaf area and photosynthetic rate averaged for genotypes increased by 71 and 41 %, respectively, with P fertilization. Significantly, higher root surface area and volume were observed in PDM-139 under low soil P. Though the grain yield was higher in ML-818, the total plant biomass was significantly higher in PDM-139 indicating improved P uptake and its efficient translation into biomass. The higher carboxylate exudation capacity and improved root traits in the later genotype might be the possible adaptive mechanisms to cope with P-stress. However, it is not necessary that higher root exudation would result in higher grain yield.     

The Response of Lupinus albus Roots to the Signal from Phosphorus-Deficient Substrate1

The excretion of organic acids into the rhizosphere is induced by low phosphorus content in roots of white lupine (Lupinus albus L.). The aim of this study was to investigate how did the white lupine roots respond to the signals of P-deficiency in the substrate, by using the method of separating the root system into two parts, one part being placed into P-deficient solution and another part into P-sufficient solution. The results showed that the root tips (1-cm-long) accept the signal of P-deficiency in the substrate. This signal can be transmitted from one root tip to another, and can induce the accumulation and excretion of malic acid in the root tips and the development of proteoid roots. In order to investigate whether a phytohormone was involved in the response, the external hormones were used. Indole-3-butyric acid added to P-sufficient solution can induce the development of proteoid roots, but without any accumulation of citric acid in them. On the contrary, 6-benzyladenine (BA) added to the P-deficient solution can inhibit the development of proteoid roots and the accumulation of malic acid in the root tips. The inhibitory effect increases with increasing BA supply.