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Journal of Arid Land  2023, Vol. 15 Issue (5): 578-601    DOI: 10.1007/s40333-023-0012-9
Research article     
Fate of rubber bush (Calotropis procera (Aiton) W. T. Aiton) in adversary environment modulated by microstructural and functional attributes
Ummar IQBAL1,*(), Mansoor HAMEED2, Farooq AHMAD2, Muhammad S AAHMAD2, Muhammad ASHRAF2
1Department of Botany, the Islamia University of Bahawalpur, Bahawalpurwala 64200, Pakistan
2Department of Botany, University of Agriculture, Faisalabad 38040, Pakistan
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Calotropis procera (Aiton) W. T. Aiton, belonging to the family Apocynaceae, is C3 evergreen plant species in arid and semi-arid areas of the Punjab Province, Pakistan. It grows in a variety of habitats like salt affected and waterlogged area, desert/semi-desert, roadside, wasteland, graveyard, forest, crop field, coastline, and river/canal bank. A total of 12 populations growing in different ecological regions were sampled to evaluate their growth, physio-biochemical, and anatomical responses to specific environmental condition. Population adapted to desert/semi-desert showed vigorous growth (plant height, shoot length, and number of leaves), enhanced photosynthetic level (chlorophyll a, chlorophyll b, carotenoids, and total chlorophyll), and apparent anatomical modifications such as increased stem radius, cuticle thickness, storage parenchyma tissues (cortex and pith), and vascular bundles in stems, while the maximum of midrib and lamina thickness, epidermal cells, cuticle thickness, cortical proportion, abaxial stomatal density, and its area in leaves. There was high plasticity in structural and functional features of these populations, which enable them to survive and tolerate under such hot and dry desert environment. Population of saline areas exhibited very critical modifications to sustain under salt prone environment. At physiological level, it possesses the maximum amount of organic osmolytes (glycine betaine and proline) and antioxidants (superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD)), while at anatomical level, it showed intensive sclerification, large phloem region (inner and outer), pith parenchyma cells, and metaxylem vessels in stems and leaves. The population of dry mountains showed very distinctive features, such as increased shoot ionic contents (K+ and Ca2+), collenchyma and sclerenchyma thickness in stems, trichomes size, and numerous small stomata on abaxial surface of leaves. It is concluded that no definite or precise single character can be taken as a yardstick for adjudging the biomass production in this rubber bush weed population.

Key wordsCalotropis procera      Apocynaceae      phenotypic plasticity      aridity      rubber bush     
Received: 24 November 2022      Published: 31 May 2023
Corresponding Authors: *Ummar IQBAL (E-mail:
Cite this article:

Ummar IQBAL, Mansoor HAMEED, Farooq AHMAD, Muhammad S AAHMAD, Muhammad ASHRAF. Fate of rubber bush (Calotropis procera (Aiton) W. T. Aiton) in adversary environment modulated by microstructural and functional attributes. Journal of Arid Land, 2023, 15(5): 578-601.

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Fig. 1 Map showing collection sites (a) of Calotropis procera populations and its habitat characteristics (b) in the Punjab Province, Pakistan. P, precipitation, E, elevation. The abbreviations of these populations are the same in the following figures and tables.
Index Stream/river channel Mountainous range Hyper-arid area Salt affected land LSD F value
Morphological trait
Plant height (m) 3.0c 2.5d 1.5f 2.0e 1.0i 2.0e 3.5b 4.1a 2.4d 2.0e 1.5f 1.5f 0.5 11.9***
Shoot length (cm) 86.4f 94.4ef 115.2d 138.2cd 150.4c 86.4f 173.8b 200.4a 100.2e 100.2e 65.2g 115.8d 15.3 4.8*
Leaf area (cm2) 213.2a 121.6d 180.0b 127.2cd 82.0ef 112.0de 129.2cd 148.8c 85.2ef 46.8f 99.6e 146.8c 25.6 11.8***
Number of leaves per shoot 108.8d 85.2e 155.4b 49.2g 129.6c 73.2ef 172.4a 57.2f 62.4f 102.4d 85.2e 124.8c 16.1 10.5***
Shoot fresh weight (g/plant) 410.8i 613.2c 664.8a 581.6d 506.4g 506.4g 633.2b 581.6d 448.4h 530.2f 448.4h 550.4e 20.5 38.9***
Shoot dry weight (g/plant) 181.2k 277.2a 182.4d 130.4f 163.2e 84.4i 104.8h 130.4f 117.2g 233.2c 260.4b 163.2e 12.5 8.0**
Plant ionic content
Shoot Na+ (mg/g d.wt.) 15.4f 29.0de 33.4d 32.2d 30.8d 27.9de 25.6e 15.4f 22.7e 67.6a 63.4ab 43.5c 7.5 20.9***
Shoot K+
(mg/g d.wt.)
20.4d 19.8e 22.0d 28.3bc 26.9c 41.1a 23.9cd 19.1e 14.2f 28.0bc 26.4c 32.7b 5.3 14.3***
Shoot Ca2+ (mg/g d.wt.) 18.9cd 18.2cd 24.5b 18.4cd 26.7ab 28.2a 16.9e 24.2b 13.8f 16.8e 21.1c 20.1c 3.4 22.2***
Photosynthetic pigment
Chlorophyll a (mg/g f.wt.) 0.91h 1.22f 1.16g 1.51d 1.37e 1.66c 0.45i 1.85a 1.72b 0.34j 0.34i 0.34i 0.30 43.8***
Chlorophyll b (mg/g f.wt.) 0.27f 0.54e 1.02b 0.77d 0.72d 0.76d 0.22g 1.12a 0.86c 0.16g 0.16g 0.16g 0.50 26.6***
Carotenoids (mg/g f.wt.) 0.04 0.02ef 0.04d 0.05cd 0.04d 0.04d 0.03de 0.08b 0.12a 0.06c 0.03de 0.01f 0.02 56.2***
Total chlorophyll (mg/g f.wt.) 1.18h 1.76g 2.18e 2.28c 2.09f 2.32d 0.67i 2.97a 2.58b 0.50j 0.50j 0.50j 0.40 30.3***
Chlorophyll a/b ratio 3.37a 2.25b 1.13g 1.96e 1.90e 2.18c 2.04d 1.65f 2.01d 2.12c 2.12c 1.70e 0.20 9.5**
Chl/Caro ratio 29.5f 88.0a 54.5c 45.6d 52.5c 58.0b 22.3g 37.1e 21.5h 8.3j 16.6i 54.0c 5.0 17.9***
Organic osmolyte
Proline (μmol/g f.wt.) 24.9d 22.5de 13.1f 22.3de 13.1f 19.7e 22.8de 25.9d 14.4 43.3a 34.0b 29.5c 4.5 23.1***
Glycine betaine (μmol/g f.wt.) 2.5bc 2.9bc 1.4cd 3.7b 3.1b 2.0c 1.0d 2.3c 1.9cd 4.9ab 5.6a 4.9ab 1.5 9.6***
Total soluble protein (μg/g f.wt.) 204.0g 333.7de 91.6i 208.2g 358.4c 102.1 320.8e 222.8fg 247.4f 127.0h 389.1b 475.6a 30.8 43.6***
(U/μg protein)
1.0d 1.4c 1.7b 1.3c 0.9de 0.7e 1.6b 1.1d 2.0a 2.0a 1.6b 1.5bc 0.3 27.5***
(U/μg protein)
1.1e 1.2e 0.8g 0.5h 1.6c 0.9fg 1.4d 1.0f 1.3d 1.8b 2.0a 1.8b 0.2 44.8***
(U/μg protein)
1.7c 1.1e 1.4d 1.0ef 0.7f 1.0ef - 1.3de 1.7c 2.1a 1.9b 1.6cd 0.2 20.1***
Table 1 Morphological and physio-biochemical traits of Calotropis procera populations growing in different habitats of the Punjab Province, Pakistan
Index Stream/river channel Mountainous range Hyper-arid area Salt affected land LSD F value
Stem radius (µm) 1696.7d 1633.3e 1918.3b 1696.7d 1696.7d 1955.8ab 1988.3a 1860.0c 1918.3b 1855.0c 1506.7f 1849.2c 59.5 2.4NS
Cuticle thickness (µm) 36.4bc 37.4bc 18.4e 31.4cd 38.4bc 40.4b 31.4cd 51.5a 26.7d 34.1c 18.4e 36.1bc 7.4 8.4**
Epidermal cell area (µm2) 425.9cd 362.7de 450.5c 231.3e 387.5d 663.5a 638.3ab 380.0d 567.3b 348.8de 638.3ab 350.2de 50.0 10.8**
Collenchyma thickness (µm) 48.8d 55.8cd 64.2c 100.7a 55.8cd 48.8d 60.9c 48.8d 75.9b 75.9b 62.6c 75.9b 10.5 8.4**
Cortical region thickness (µm) 168.3b 168.3b 83.5cd 84.8cd 96.2c 58.9d 79.3cd 198.9a 168.3b 90.0c 108.0c 106.0c 32.7 15.1***
Cortical cell area (µm2) 212.0b 90.1e 35.2f 35.2f 105.5d 153.2c 78.6e 252.2a 142.1c 78.5e 99.5d 143.9c 33.3 28.2***
Sclerenchyma thickness (µm) 564.2d 775.0ab 664.6c 693.3b 790.4a 700.4b 300.0g 400.0f 263.3h 303.0g 790.4a 511.0e 28.9 1.1NS
Metaxylem area (µm2) 41.8ef 105.5c 102.1c 99.0c 73.6d 96.7c 247.0a 50.0e 71.7d 201.2b 23.5f 118.8c 34.1 28.3***
Outer phloem area (µm2) 58.3e 166.7d 244.2c 453.6b 105.5d 136.7d 229.4c 588.9a 180.6cd 588.9a 118.5d 214.5c 80.8 24.7***
Inner phloem area (µm2) 85.2f 193.2d 204.2d 326.2c 156.7de 85.2f 160.0de 312.9c 203.3d 431.1b 116.6e 503.0a 89.1 20.2***
Pith thickness (µm) 216.1c 111.3e 298.9b 183.3d 249.8bc 170.3d 352.1a 217.9c 214.6c 298.9b 111.3e 186.0d 49.3 14.1***
Pith cell area (µm2) 163.2c 41.4g 106.2e 148.3c 73.6f 158.5c 132.6d 217.2a 127.4d 217.2a 97.5e 190.0b 31.0 11.8**
Table 2 Stem anatomical traits of Calotropis procera populations growing in different habitats of the Punjab Province, Pakistan
Fig. 2 Transverse sections showing different stems tissues of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan
Index Stream/river channel Mountainous range Hyper-arid area Salt affected land LSD F value
Midrib thickness (µm) 5517.9a 4273.7c 2288.3g 3365.6f 4132.1d 4135.4d 5517.9a 4398.3b 1198.3h 1018.3i 3796.2e 1195.0h 500.9 272.3***
Lamina thickness (µm) 176.1e 103.9g 198.9c 83.2h 223.6bc 176.4e 183.3d 246.5a 232.1b 194.7c 132.0f 133.8f 11.2 80.4***
Epidermal cell area (µm2) 16.2g 39.3e 16.2g 20.1f 85.0bc 21.6f 101.0a 85.9bc 74.3c 89.3b 46.0d 84.3bc 4.7 201.5***
Cuticle thickness (µm) 28.8c 32.0b 13.0f 33.4ab 19.3d 16.0e 18.7d 35.3a 28.0c 18.8d 35.3a 33.4ab 2.7 34.3***
chyma thickness (µm)
723.0c 771.3b 147.8j 155.4i 296.8h 504.3e 501.5e 154.5i 448.1f 313.0g 846.5a 548.4d 39.4 104.2***
Cortical thickness (µm) 990.5b 641.6d 896.6c 389.9g 614.0de 610.4de 1067.7a 262.8h 672.4d 853.0c 567.8e 470.4f 75.8 42.3***
Cortical cell area (µm2) 385.3b 251.2e 161.3h 231.4f 176.3g 260.7e 432.0a 294.3d 176.5g 146.6i 307.7c 432.0a 21.3 530.6***
Metaxylem area (µm2) 530.1b 608.5ab 511.5bc 423.4c 183.4f 266.1e 633.2a 583.6ab 443.2c 364.3d 537.7b 493.8bc 76.1 19.0***
Phloem area (µm2) 139.4g 301.2a 161.3f 101.9i 101.9i 232.9d 166.7f 285.3b 115.6h 172.6e 242.7c 301.2a 23.2 303.3***
Trichome area (µm2) 137.8h 261.4c 207.3e 355.2a 108.1i 144.4g 81.2j 280.1b 61.9k 258.1d 174.9f 81.7j 19.8 929.3***
Trichome density (individu-
52.6f 79.9d 49.3g 100.8b 49.9g 69.3e 49.5g 119.2a 40.5h 85.3c 40.5h 90.3c 6.6 151.0***
Adaxial stomatal area (µm2) 914.2b 827.7d 957.3a 432.2j 700.8g 685.1h 682.6h 796.0e 718.0f 496.3i 795.5e 861.4c 21.0 1657.5***
Abaxial stomatal area (µm2) 842.9b 524.4d 737.0c 100.3i 83.8j 100.2i 269.0g 881.4a 83.8j 121.5h 508.6e 404.9f 20.5 3545.1***
Adaxial stomatal density (individu-
35.0d 50.0a 45.0b 40.0c 35.0d 32.0de 32.0de 23.0f 29.0e 26.0ef 31.0e 28.0e 5.8 100.2***
Abaxial stomatal density (individu-
27.0b 26.0b 29.0ab 21.0c 31.0a 16.0d 20.0c 31.0a 27.0b 21.0c 29.0ab 29.0ab 3.2 73.9***
Table 3 Leaf anatomical traits of Calotropis procera populations growing in different habitats of the Punjab Province, Pakistan
Fig. 3 Transverse sections showing different leaf tissues of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan
Fig. 4 Transverse sections showing epidermal surface view of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan
Fig. 5 PCA (principle component analysis) showing association of soil physical-chemical characteristics with growth (a), physiology (b), stem (c), and leaf anatomical attributes (d) of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan. PH, plant height; LN, number of leaves; LA, leaf area; SL, shoot length; SFW, shoot fresh weight; SDW, shoot dry weight; SNa+, shoot Na+; SK+, shoot K+; SCa2+, shoot Ca2+; Chla, Chlorophyll a; Chlb, Chlorophyll b; Caro, carotenoids; Tchl, total chlorophyll; Pro, proline; GB, glycine betaine; TSP, total soluble proteins; SOD, superoxide dismutase; CAT, catalase; POD, peroxidase; Ca2+, soil Ca2+; K+, soil K+; Na+, soil Na+; Cl?, soil Cl?; EC, electrochemical conductivity; pH, soil pH; CuT, cuticle thickness; StR, stem radius; CCA, cortical cell area; EpCA, epidermal cell area; CRT, cortical thickness; SCT, sclerenchymatous thickness; ColT, collenchymatous thickness; IPA, inner phloem area; OPA, outer phloem area; PCA', epidermal cell area; MtA, metaxylem area; PhlA, phloem area; TA, trichome area; TD, trichome density; LmT, lamina thickness; AdSD, adaxial stomatal density; CorT, cortical region thickness; AdSA, adaxial stomatal area; AbSA, abaxial stomatal area; AbSD, abaxial stomatal density; MrbT, midrib thickness. The abbreviations are the same in figures 6, 7 and 8.
Fig. 6 (a), correlation among soil physical-chemical traits and morpho-physiological attributes, and (b), density heatmap for soil physical-chemical traits and morpho-physiological attributes of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan. *, P<0.05 level; ***, P<0.01 level.
Fig. 7 (a), correlation among soil physical-chemical traits and stem structural attributes; (b), cluster heatmap for soil physical-chemical traits and stem structural attributes of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan. *, P<0.05 level; **, P<0.01 level; ***, P<0.001 level.
Fig. 8 (a), correlation among soil physical-chemical traits and leaf structural attributes; (b), cluster heatmap for soil physical-chemical traits and leaf structural attributes of Calotropis procera populations collected from different habitats of the Punjab Province, Pakistan. *, P<0.05 level; **, P<0.01 level; ***, P<0.001 level.
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