Fate of rubber bush (<i>Calotropis procera</i> (Aiton) W. T. Aiton) in adversary environment modulated by microstructural and functional attributes

doi:10.1007/s40333-023-0012-9

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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Abstract

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 words： Calotropis procera Apocynaceae phenotypic plasticity aridity rubber bush

Received: 24 November 2022 Published: 31 May 2023

Corresponding Authors: *Ummar IQBAL (E-mail: ummariqbal@yahoo.com)

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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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http://jal.xjegi.com/10.1007/s40333-023-0012-9 OR http://jal.xjegi.com/Y2023/V15/I5/578

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
Index	KHP		TBJ	ADS	PCK	PDK	NSR	DIS	AHP	DGK	LSH	KBL	KKL	LSD		F value
Morphological trait
Plant height (m)	3.0^c		2.5^d	1.5^f	2.0^e	1.0ⁱ	2.0^e	3.5^b	4.1^a	2.4^d	2.0^e	1.5^f	1.5^f	0.5	11.9^***
Shoot length (cm)	86.4^f		94.4^ef	115.2^d	138.2^cd	150.4^c	86.4^f	173.8^b	200.4^a	100.2^e	100.2^e	65.2^g	115.8^d	15.3	4.8^*
Leaf area (cm²)	213.2^a		121.6^d	180.0^b	127.2^cd	82.0^ef	112.0^de	129.2^cd	148.8^c	85.2^ef	46.8^f	99.6^e	146.8^c	25.6	11.8^***
Number of leaves per shoot	108.8^d		85.2^e	155.4^b	49.2^g	129.6^c	73.2^ef	172.4^a	57.2^f	62.4^f	102.4^d	85.2^e	124.8^c	16.1	10.5^***
Shoot fresh weight (g/plant)	410.8ⁱ		613.2^c	664.8^a	581.6^d	506.4^g	506.4^g	633.2^b	581.6^d	448.4^h	530.2^f	448.4^h	550.4^e	20.5	38.9^***
Shoot dry weight (g/plant)	181.2^k		277.2^a	182.4^d	130.4^f	163.2^e	84.4ⁱ	104.8^h	130.4^f	117.2^g	233.2^c	260.4^b	163.2^e	12.5	8.0^**
Plant ionic content
Shoot Na⁺ (mg/g d.wt.)		15.4^f	29.0^de	33.4^d	32.2^d	30.8^d	27.9^de	25.6^e	15.4^f	22.7^e	67.6^a	63.4^ab	43.5^c	7.5	20.9^***
Shoot K⁺ (mg/g d.wt.)		20.4^d	19.8^e	22.0^d	28.3^bc	26.9^c	41.1^a	23.9^cd	19.1^e	14.2^f	28.0^bc	26.4^c	32.7^b	5.3	14.3^***
Shoot Ca²⁺ (mg/g d.wt.)		18.9^cd	18.2^cd	24.5^b	18.4^cd	26.7^ab	28.2^a	16.9^e	24.2^b	13.8^f	16.8^e	21.1^c	20.1^c	3.4	22.2^***
Photosynthetic pigment
Chlorophyll a (mg/g f.wt.)		0.91^h	1.22^f	1.16^g	1.51^d	1.37^e	1.66^c	0.45ⁱ	1.85^a	1.72^b	0.34^j	0.34ⁱ	0.34ⁱ	0.30	43.8^***
Chlorophyll b (mg/g f.wt.)		0.27^f	0.54^e	1.02^b	0.77^d	0.72^d	0.76^d	0.22^g	1.12^a	0.86^c	0.16^g	0.16^g	0.16^g	0.50	26.6^***
Carotenoids (mg/g f.wt.)		0.04	0.02^ef	0.04^d	0.05^cd	0.04^d	0.04^d	0.03^de	0.08^b	0.12^a	0.06^c	0.03^de	0.01^f	0.02	56.2^***
Total chlorophyll (mg/g f.wt.)		1.18^h	1.76^g	2.18^e	2.28^c	2.09^f	2.32^d	0.67ⁱ	2.97^a	2.58^b	0.50^j	0.50^j	0.50^j	0.40	30.3^***
Chlorophyll a/b ratio		3.37^a	2.25^b	1.13^g	1.96^e	1.90^e	2.18^c	2.04^d	1.65^f	2.01^d	2.12^c	2.12^c	1.70^e	0.20	9.5^**
Chl/Caro ratio		29.5^f	88.0^a	54.5^c	45.6^d	52.5^c	58.0^b	22.3^g	37.1^e	21.5^h	8.3^j	16.6ⁱ	54.0^c	5.0	17.9^***
Organic osmolyte
Proline (μmol/g f.wt.)		24.9^d	22.5^de	13.1^f	22.3^de	13.1^f	19.7^e	22.8^de	25.9^d	14.4	43.3^a	34.0^b	29.5^c	4.5	23.1^***
Glycine betaine (μmol/g f.wt.)		2.5^bc	2.9^bc	1.4^cd	3.7^b	3.1^b	2.0^c	1.0^d	2.3^c	1.9^cd	4.9^ab	5.6^a	4.9^ab	1.5	9.6^***
Total soluble protein (μg/g f.wt.)		204.0^g	333.7^de	91.6ⁱ	208.2^g	358.4^c	102.1	320.8^e	222.8^fg	247.4^f	127.0^h	389.1^b	475.6^a	30.8	43.6^***
Antioxidant
SOD (U/μg protein)		1.0^d	1.4^c	1.7^b	1.3^c	0.9^de	0.7^e	1.6^b	1.1^d	2.0^a	2.0^a	1.6^b	1.5^bc	0.3	27.5^***
CAT (U/μg protein)		1.1^e	1.2^e	0.8^g	0.5^h	1.6^c	0.9^fg	1.4^d	1.0^f	1.3^d	1.8^b	2.0^a	1.8^b	0.2	44.8^***
POD (U/μg protein)		1.7^c	1.1^e	1.4^d	1.0^ef	0.7^f	1.0^ef	-	1.3^de	1.7^c	2.1^a	1.9^b	1.6^cd	0.2	20.1^***

Table 1 Morphological and physio-biochemical traits of Calotropis procera populations growing in different habitats of the Punjab Province, Pakistan

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
Index	KHP	TBJ	ADS	PCK	PDK	NSR	DIS	AHP	DGK	LSH	KBL	KKL	LSD	F value
Midrib thickness (µm)	5517.9^a	4273.7^c	2288.3^g	3365.6^f	4132.1^d	4135.4^d	5517.9^a	4398.3^b	1198.3^h	1018.3ⁱ	3796.2^e	1195.0^h	500.9	272.3^***
Lamina thickness (µm)	176.1^e	103.9^g	198.9^c	83.2^h	223.6^bc	176.4^e	183.3^d	246.5^a	232.1^b	194.7^c	132.0^f	133.8^f	11.2	80.4^***
Epidermal cell area (µm²)	16.2^g	39.3^e	16.2^g	20.1^f	85.0^bc	21.6^f	101.0^a	85.9b^c	74.3^c	89.3^b	46.0^d	84.3^bc	4.7	201.5^***
Cuticle thickness (µm)	28.8^c	32.0^b	13.0^f	33.4^ab	19.3^d	16.0^e	18.7^d	35.3^a	28.0^c	18.8^d	35.3^a	33.4^ab	2.7	34.3^***
Scleren- chyma thickness (µm)	723.0^c	771.3^b	147.8^j	155.4ⁱ	296.8^h	504.3^e	501.5^e	154.5ⁱ	448.1^f	313.0^g	846.5^a	548.4^d	39.4	104.2^***
Cortical thickness (µm)	990.5^b	641.6^d	896.6^c	389.9^g	614.0^de	610.4^de	1067.7^a	262.8^h	672.4^d	853.0^c	567.8^e	470.4^f	75.8	42.3^***
Cortical cell area (µm²)	385.3^b	251.2^e	161.3^h	231.4^f	176.3^g	260.7^e	432.0^a	294.3^d	176.5^g	146.6ⁱ	307.7^c	432.0^a	21.3	530.6^***
Metaxylem area (µm²)	530.1^b	608.5^ab	511.5^bc	423.4^c	183.4^f	266.1^e	633.2^a	583.6^ab	443.2^c	364.3^d	537.7^b	493.8^bc	76.1	19.0^***
Phloem area (µm²)	139.4^g	301.2^a	161.3^f	101.9ⁱ	101.9ⁱ	232.9^d	166.7^f	285.3^b	115.6^h	172.6^e	242.7^c	301.2^a	23.2	303.3^***
Trichome area (µm²)	137.8^h	261.4^c	207.3^e	355.2^a	108.1ⁱ	144.4^g	81.2^j	280.1^b	61.9^k	258.1^d	174.9^f	81.7^j	19.8	929.3^***
Trichome density (individu- als/mm²)	52.6^f	79.9^d	49.3^g	100.8^b	49.9^g	69.3^e	49.5^g	119.2^a	40.5^h	85.3^c	40.5^h	90.3^c	6.6	151.0^***
Adaxial stomatal area (µm²)	914.2^b	827.7^d	957.3^a	432.2^j	700.8^g	685.1^h	682.6^h	796.0^e	718.0^f	496.3ⁱ	795.5^e	861.4^c	21.0	1657.5^***
Abaxial stomatal area (µm²)	842.9^b	524.4^d	737.0^c	100.3ⁱ	83.8^j	100.2ⁱ	269.0^g	881.4^a	83.8^j	121.5^h	508.6^e	404.9^f	20.5	3545.1^***
Adaxial stomatal density (individu- als/mm²)	35.0^d	50.0^a	45.0^b	40.0^c	35.0^d	32.0^de	32.0^de	23.0^f	29.0^e	26.0^ef	31.0^e	28.0^e	5.8	100.2^***
Abaxial stomatal density (individu- als/mm²)	27.0^b	26.0^b	29.0^ab	21.0^c	31.0^a	16.0^d	20.0^c	31.0^a	27.0^b	21.0^c	29.0^ab	29.0^ab	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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