Biodiversity Science ›› 2013, Vol. 21 ›› Issue (6): 715-722.doi: 10.3724/SP.J.1003.2013.08152

• Orginal Article • Previous Article     Next Article

Diversity of calcium speciation in leaves of Primulina species (Gesneriaceae)

Qingwen Qi1, 2, Zhuan Hao1, 2, Junjie Tao1, 2, Ming Kang1, *()   

  1. 1 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650
    2 University of the Chinese Academy of Sciences, Beijing 100049
  • Received:2013-07-03 Accepted:2013-10-28 Online:2013-12-02
  • Kang Ming

Primulina is a genus containing typical “stone plants” or “cave plants” that show a high degree of edaphic specialization in the karst limestone regions of southwest China. Most species of the genus occur only on calcareous soils developed from carbonate bedrock, while a few species are found only on the red soil developed from the Danxia landform or acidic soil developed from sandshale bedrock. The aim of this study is to investigate the diversity and characteristics of calcium absorption and storage in Primulina from different soil substrates. Calcium in leaves was determined for plants sampled from 15 populations representing 11 Primulina species occurring on calcareous soil, red soil or acid soil. We analyzed the main types of calcium found in leaves, and compared the calcium content within and among species from different soil types. The results revealed a general high level of leaf calcium content in Primulina species compared with other plants from the karst regions of southwest China. However, we found a significant difference in calcium content among Primulina species from different soil types, with high average calcium content (2,285.6 mg/kg) in Primulina from calcareous soil relative to low levels present in Primulina from both acid soil (1,379.3 mg/kg) and Danxia red soil (1,329.1 mg/kg). The main form of calcium stored in most Primulina species (9 out of 11) was pectate calcium, which accounted for 31.6-64.2% of the total calcium in the leaves. In contrast, for two species, P. linearifolia and P. medica, which grow on soil with a pH > 8, the main calcium form was soluble calcium, which accounted for about 40% of the total calcium in plant leaves. In addition, differences in calcium amount and type were recorded within species from either the same or different soil types. These results suggest that there is variation in calcium speciation found in Primulina at both interspecific and intraspecific levels. Our findings provide a valuable basis for further studies on adaptive mechanisms of edaphic specialization in Primulina.

Key words: Primulina, karst plant, calcareous soil, acidic soil, calcium speciation, diversity

Table 1

Sampling information of the 15 Primulina populations in this study"

Bedrocks and code
Sampling locations
土壤 pH
Soil pH
石灰岩 Limestone
ZJHZ01 西子报春苣苔 Primulina xiziae 浙江杭州 Hangzhou, Zhejiang -
DX03 牛耳朵 P. eburnean 湖南道县 Daoxian, Hunan 7.5
HNBT03 烟叶报春苣苔 P. heterotricha 海南保亭县 Baoting, Hainan 7.2
YLY01 线叶报春苣苔 P. linearifolia 广西武鸣县 Wuming, Guangxi 8.1
GXQT01 药用报春苣苔 P. medica 广西平乐县 Pingle, Guangxi 8.0
丹霞地貌 Danxia
GXRX01 钟冠报春苣苔 P. swinglei 广西容县 Rongxian, Guangxi 7.8
GDLC07 报春苣苔属一新种 Primulina sp. 广东乐昌 Lechang, Guangdong 7.7
DXS05 蚂蝗七 P. fimbrisepala 广东丹霞山 Danxia, Guangdong 7.6
GXZY01 蚂蝗七 P. fimbrisepala 广西资源县 Ziyuan, Guangxi 5.0
砂页岩 Sandshale
GDSZ01 中华报春苣苔 P. sinensis 广东深圳 Shenzhen, Guangdong 4.3
HNBT01 烟叶报春苣苔 P. heterotricha 海南保亭县 Baoting, Hainan 5.5
WG02 蚂蝗七 P. fimbrisepala 湖南武冈市 Wugang, Hunan 3.6
CBL01 蚂蝗七 P. fimbrisepala 广东始兴县 Shixing, Guangdong 3.8
LBJX01 齿萼报春苣苔 P. verecunda 广西金秀县 Jinxiu, Guangxi 3.3
GZJK01 钝齿报春苣苔 P. obtusidentata 贵州江口县 Jiangkou, Guizhou 4.2

Table 2

Extraction procedure and chemical fraction of calcium speciation in leaves"

Extraction order
Extraction solution
Calcium speciation
1 80% C2H5OH 硝酸钙与氯化钙 Calcium nitrate and calcium chloride AIC-Ca
2 Distilled water 水溶性有机酸钙 Water soluble calcium H2O-Ca
3 1 M NaCl 果胶酸钙 Calcium pectate NaCl-Ca
4 2% CH3COOH 磷酸钙与碳酸钙 Calcium phosphate and calcium carbonate HAC-Ca
5 0.6% HCl 草酸钙 Calcium oxalate HCl-Ca
残渣 Residual - 残渣钙(硅酸钙) Silicate calcium Res-Ca

Table 3

Average contents of calcium speciation and total calcium content (mg/kg) in leaves of Primulina from different soil types. The values in the parentheses represent the standard errors."

果胶酸钙 NaCl-Ca 水溶性钙
硝酸钙和氯化钙 AIC-Ca 磷酸钙和碳酸钙
Total calcium
石灰岩 Limestone 959.4(90.1)A 710.6(197.9)A 437.8(80.9)A 82.7(12.1) 23.5(4.3)A 71.5(13.8)A 2,285.6(292.8)A
丹霞地貌 Danxia 733.0(95.3)B 296.5(58.0)B 137.1(28.1)C 83.2(22.7) 20.0(3.2)AB 59.2(10.4)B 1,329.1(133.2)B
砂页岩 Sandshale 691.5(54.5)B 287.0(53.4)B 241.3(32.4)B 83.0(10.2) 17.8(2.5)B 58.7(6.0)B 1,379.3(112.1)B

Table 4

Content of various calcium speciation (mg/kg) in leaves of the 15 Primulina populations. The values in the parentheses represent the standard errors."

ZJHZ01 1,148.7(78.0)A 617.5(6.5)C 564.6(44.9)B 62.7(3.7)EF 19.8(0.7)EF 128.3(1.4)A
DX03 1,132.5(31.0)A 354.4(9.1)F 128.3(2.7)F 72.7(3.1)ED 40.5(1.6)A 35.1(1.3)G
HNBT03 656.1(25.1)D 243.7(6.6)H 530.8(5.4)B 69.0(0.5)ED 13.6(1.0)HJ 57.5(3.4)E
YLY01 782.8(10.7)C 847.9(16.0)B 342.8(9.3)C 73.0(1.2)ED 26.9(1.6)CB 65.0(1.6)ED
GXQT01 1,076.9 (16.0)A 1,489.6(53.9)A 622.7(41.7)A 136.3(5.4)B 16.7(0.9)HFG 71.6(1.3)D
GXRX01 427.0(14.1)F 160.8(9.3)I 224.4(6.4)D 39.0(2.5)G 10.1(0.3)J 72.8(0.7)CD
GDLC07 748.5(8.8)C 366.6(12.6)EF 68.3(2.8)G 158.2(8.9)A 27.2(1.4)CB 45.2(7.8)F
DXS05 811.0(6.3)C 210.4(5.2)IH 136.1(4.9)F 78.7(2.3)D 24.0(1.5)CD 33.4(1.0)G
GXZY01 945.7(15.2)B 448.3(11.8)D 119.6(1.9)G 57.0(1.7)F 18.8(1.1)EFG 85.4(0.8)B
GDSZ01 746.2(8.4)C 369.1(6.3)EF 351.7(3.7)C 126.7(2.7)B 9.1(0.3)J 48.6(2.1)F
HNBT01 514.8(10.7)E 298.1(5.8)G 206.7(5.0)ED 40.8(0.5)G 15.4(0.5)HG 68.1(2.0)D
WG02 902.9(7.0)B 416.2(9.5)ED 144.2(1.5)F 99.4(1.4)C 21.9(0.5)ED 71.2(1.7)D
CBL01 644.2(4.4)D 181.9(1.4)I 162.1(1.8)EF 69.1(0.4)ED 10.7(0.3)JI 35.6(0.5)G
LBJX01 816.5(2.2)C 425.8(2.1)D 249.1(0.7)D 90.5(1.3)C 22.3(0.8)ED 47.7(0.5)F
GZJK01 524.5(3.7)E 30.6(0.3)J 334.0(4.1)C 71.2(0.5)ED 27.8(0.5)B 81.0(1.3)CB

Fig. 1

Percentage of various calcium speciation of leaves for the 15 Primulina populations. Population codes and abbreviations of calcium speciation as shown in Table 1 and Table 2, respectively."

Table 5

Comparison of calcium speciation concentration in leaves of Primulina fimbrisepala and Primulina heterotricha from different bedrocks. The values in the parentheses represent standard errors."

水溶性钙H2O-Ca 硝酸钙
Total calcium
878.3(25.2) 329.4(42.6) 127.9(3.9)B 67.9(4.1)B 21.4(1.3) 59.4(26.0) 1,484.2(67.9)
773.5(45.9) 299.0(41.7) 153.2(3.4)A 84.3(5.4)A 16.3(2.0) 53.4(6.4) 1,379.7(97.8)
HNBT03 656.1(25.1)A 243.7(6.6)B 530.8(5.4)A 69.0(0.5)A 13.6(1.0) 57.5(3.4) 1,570.6(21.0)
HNBT01 514.8(10.7)B 298.1(5.8)A 206.7(5.0)B 40.8(0.5)B 15.4(0.5) 68.1(2.0) 1,144.0(6.7)
1 Cao JH (曹建华), Yuan DX (袁道先), Pan GX (潘根兴) (2003) Some soil features in karst ecosystem.Advance in Earth Sciences(地球科学进展), 18, 37-44. (in Chinese with English abstract)
2 Cao JH (曹建华), Zhu MJ (朱敏洁), Huang F (黄芬), Lu Q (卢茜) (2011) Comparison study on calcium forms in plant leaves under different geological backgrounds: a case study in Maolan, Guizhou Province. Bulletin of Mineralogy,Petrology and Geochemistry(矿物岩石地球化学通报), 30, 251-260. (in Chinese with English abstract)
3 Clark JL, Funke MM, Duffy AM, Smith JF (2012) Phylogeny of a neotropical clade in the Gesneriaceae: more tales of convergent evolution.International Journal of Plant Sciences, 173, 894-916.
4 Dunjo G, Pardini G, Gispert M (2003) Land use change effects on abandoned terraced soils in a Mediterranean catchment, NE Spain.Catena, 52, 23-37.
5 Edwards PJ, Grubb PJ (1982) Studies of mineral cycling in a montane rain-forest in New-Guinea. 4. Soil characteristics and the division of mineral elements between the vegetation and soil.Journal of Ecology, 70, 649-666.
6 Fahn A (1986) Structural and functional properties of trichomes of xeromorphic leaves.Annals of Botany, 57, 631-637.
7 Feng XY (冯晓英), Hu ZP (胡章平), Yi Y (乙引) (2010) Variation of proline and soluble protein content in leaves of Eurycorymbus cavalerieian and Pinus armandii under Ca2+ stress.Guizhou Agricultural Science(贵州农业科学), 38, 169-170. (in Chinese with English abstract)
8 Francesch VR, Nakata PA (2005) Calcium oxalate in plants: formation and function.Annual Review of Plant Biology, 56, 41-71.
9 Hepler PK, Wayne RO (1985) Calcium and plant development.Annual Review of Plant Physiology, 36, 397-439.
10 Hu LN (胡乐宁), Su YR (苏以荣), He XY (何寻阳), Li Y (李扬), Li L (黎蕾), Wang YH (王嫒华), Wu JS (吴金水) (2012) The speciation and content of calcium in karst soil, and its effects on soil organic carbon in Karst region of southwest China.Scientia Agricultura Sinica(中国农业科学), 45, 1946-1953. (in Chinese with English abstract)
11 Jefferies RL, Willis AJ (1964) Studies on the calcicole- calcifuge habit: II. The influence of calcium on the growth and establishment of four species in soil and sand cultures.Journal of Ecology, 52, 691-707.
12 Ji FT (姬飞腾), Li N (李楠), Deng X (邓馨) (2009) Calcium contents and high calcium adaptation of plants in karst areas of China.Journal of Plant Ecology(植物生态学报), 33, 926-935. (in Chinese with English abstract)
13 Kinzel H (1989) Calcium in the vacuoles and cell-walls of plant-tissue-forms of deposition and their physiological and ecological significance.Flora, 182, 99-125.
14 Li FL (李芳兰), Bao WK (包维楷) (2005) Responses of the morphological and anatomical structure of the plant leaf to environmental change.Chinese Bulletin of Botany(植物学通报), 22, 118-127. (in Chinese with English abstract)
15 Li QY (李青云), Ge HB (葛会波), Hu SM (胡淑明), Wang HY (王惠英) (2006) Effects of sodium and calcium salt stresses on strawberry photosynthesis.Acta Botanica Boreali-Occidentalia Sinica(西北植物学报), 26, 1713-1717. (in Chinese with English abstract)
16 Lu SN (陆仕念), Fu LF (符龙飞), Liang GY (梁桂友), Wen F (温放) (2013) Primulina bullata, a new species of Primulina (Gesneriaceae) from Guangxi.Guihaia(广西植物), 33, 42-45. (in Chinese with English abstract)
17 Mazen AMA (2004) Calcium oxalate deposits in leaves of Corchorus olitorius as related to accumulation of toxic metals.Russian Journal of Plant Physiology, 51, 281-285.
18 Ohat Y, Yamamoto K, Deguchi M (1970) Chemical fractionation of calcium in the fresh rice leaf blade and influences of deficiency or oversupply of calcium and age of leaf on the content of each calcium fraction: chemical fractionation of calcium in some plant species (Part 1). Journal of the Science of Soil and Manure, Japan, 41, 19-26. (in Japanese)
19 Paul A, Hauck M, Leuschner C (2009) Iron and phosphate uptake explains the calcifuge-calcicole behavior of the terricolous lichens Cladonia furcata subsp. furcata and C. rangiformis. Plant and Soil, 319, 49-56.
20 Pennisi SV, McConnell DB (2001) Inducible calcium sinks and preferential calcium allocation in leaf primordia of Dracaena sanderiana Hort. Sander ex M. T. Mast. (Dracaenaceae).Hortscience, 36, 1187-1191.
21 Ren H, Zhang Q, Wang Z, Guo Q, Wang J, Liu N, Liang K (2010) Conservation and possible reintroduction of an endangered plant based on an analysis of community ecology: a case study of Primulina tabacum Hance in China.Plant Species Biology, 25(1), 43-50.
22 Said A, Damiani A, Ma G, Kalthoff D, Beer M, Osterrieder N (2011) An equine herpesvirus 1 (EHV-1) vectored H1 vaccine protects against challenge with swine-origin influenza virus H1N1.Veterinary Microbiology, 154, 113-123.
23 Tyler G (2003) Some ecophysiological and historical appro- aches to species richness and calcicole/calcifuge behav- iour—contribution to a debate.Folia Geobotanica, 38, 419-428.
24 Tyler G, Strom L (1995) Differing organic acid exudation pattern explains calcifuge and acidifuge behaviour of plants.Annals of Botany, 75, 75-78.
25 White PJ, Broadley MR (2003) Calcium in plants.Annals of Botany, 92, 487-511.
26 Yang C (杨成), Liu CQ (刘丛强), Song ZL (宋照亮), Liu ZM (刘占民) (2007) Characteristics of the nutrient element contents in plants from Guizhou karst mountainous area of China.Ecology and Environment(生态环境), 16, 503-508. (in Chinese with English abstract)
27 Yang S (杨珊), He XY (何寻阳), Su YR (苏以荣), Zhang W (张伟), Wang KL (王克林) (2010) Effects of parent rock and land use pattern on soil fertility in Karst region of Northwest.Chinese Journal of Applied Ecology(应用生态学报), 21, 1596-1602. (in Chinese with English abstract)
28 Zhou W (周卫), Wang H (汪洪) (2007) The physiological and molecular mechanisms of calcium uptake, transport, and metabolism in plants.Chinese Bulletin of Botany(植物学通报), 24, 762-778. (in Chinese with English abstract)
29 Zhou ZB (周智彬), Li PJ (李培军) (2002) A review on the phytotomy research of xerophytes in China.Arid Zone Research(干旱区研究), 19, 35-40. (in Chinese with English abstract)
30 Zindler-Frank E, Hönow R, Hesse A (2001) Calcium and oxalate content of the leaves of Phaseolus vulgaris at different calcium supply in relation to calcium oxalate crystal formation.Journal of Plant Physiology, 158, 139-144.
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