Please wait a minute...
Journal of Arid Land  2019, Vol. 11 Issue (6): 795-810    DOI: 10.1007/s40333-019-0016-7
Orginal Article     
Mesophyll thickness and sclerophylly among Calotropis procera morphotypes reveal water-saved adaptation to environments
Marcelo F POMPELLI1,*(), Keila R MENDES1, Marcio V RAMOS2, José N B SANTOS1, Diaa T A YOUSSEF3, Jaqueline D PEREIRA4, Laurício ENDRES5, Alfredo JARMA-OROZCO6, Rodolfo SOLANO-GOMES7, Betty JARMA-ARROYO6, André L J SILVA5, Marcos A SANTOS1, Werner C ANTUNES8
1 Plant Physiology Laboratory, Department of Botany, Federal University of Pernambuco, Recife 50670901, Brazil
2 Department of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza 60020603, Brazil
3 Department of Natural Products, Faculty of Pharmacy, King Abdulaziz University, Jeddah 21589, Saudi Arabia
4 Institute of Botany, Federal University of Vi?osa, Rio Paranaíba Campus, Rio Paranaiba 36570900, Brazil
5 Plant Ecophysiology Laboratory, Federal University of Alagoas, Maceio 57072900, Brazil
6 Faculty of Agricultural Science, University of Córdoba, Montería 230002, Colombia
7 Instituto Politécnico Nacional, Research Interdisciplinary Center for Integrated Rural Development, Santa Cruz Xoxocotlan, Oaxaca 7738, Mexico
8 Department of Biology, University of Maringá, Maringá 87020900, Brazil
Download: HTML     PDF(3195KB)
Export: BibTeX | EndNote (RIS)      

Abstract  

Calotropis procera (Aiton) Dryand (Apocynaceae) is a native species in tropical and subtropical Africa and Asia. However, due to its fast growing and drought-tolerant, it has become an invasive species when it was introduced into Central and South America, as well as the Caribbean Islands. Currently, C. procera displays a wide distribution in the world. Invasiveness is important, in particular, because many invasive species exert a high reproductive pressure on the invaded communities or are highly productive in their new distributed areas. It has been suggested that a very deep root system and a high capacity to reduce stomatal conductance during water shortage could allow this species to maintain the water status required for a normal function. However, the true mechanism behind the successful distribution of C. procera across wet and dry environments is still unknown. C. procera leaves were collected from 12 natural populations in Brazil, Colombia and Mexico, ranging from wet to dry environments during 2014-2015. Many traits of morphology and anatomy from these distinct morphotypes were evaluated. We found that C. procera leaves had a considerable capacity to adjust their morphological, anatomical and physiological traits to different environments. The magnitude of acclimation responses, i.e., plasticity, had been hypothesized to reflect the specialized adaptation of plant species to a particular environment. However, allometric models for leaf area (LA) estimation cannot be grouped as a single model. Leaves are narrower and thicker with low amounts of air spaces inside the leaf parenchyma in wet environments, while they are broader and thinner with a small number of palisade cell layers in dry environments. Based on these, we argue that broader and thinner leaves of C. procera dissipate incident energy at the expense of a higher rate of transpiration to survive in environments in which water is the most limiting factor and to compete in favorable wet environments.



Key wordsinvasive plant      energy budget      leaf anatomy      morphological trait      specific leaf area     
Received: 07 July 2018      Published: 10 December 2019
Corresponding Authors:
Cite this article:

Marcelo F POMPELLI, Keila R MENDES, Marcio V RAMOS, José N B SANTOS, Diaa T A YOUSSEF, Jaqueline D PEREIRA, Laurício ENDRES, Alfredo JARMA-OROZCO, Rodolfo SOLANO-GOMES, Betty JARMA-ARROYO, André L J SILVA, Marcos A SANTOS, Werner C ANTUNES. Mesophyll thickness and sclerophylly among Calotropis procera morphotypes reveal water-saved adaptation to environments. Journal of Arid Land, 2019, 11(6): 795-810.

URL:

http://jal.xjegi.com/10.1007/s40333-019-0016-7     OR     http://jal.xjegi.com/Y2019/V11/I6/795

1 Alberio C, Comparatore V. 2014. Patterns of woody plant invasion in an Argentinean coastal grassland. Acta Oecologia, 54(1): 65-71.
2 Antunes W C, Pompelli M F, Carretero D M, et al. 2008. Allometric models for non-destructive leaf area estimation in coffee (Coffea arabica and Coffea canephora). Annals of Applied Biology, 153(1): 33-40.
3 Antunes W C, Daloso D M, Pinheiro D P, et al. 2017. Guard cell-specific down-regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environmental Experimental Botany, 135(1): 73-85.
4 Arterburn M A, Jones S S, Kidwell K K.2010. Plant breeding and genetics. In: Verheye W H. Soils, Plant Growth and Crop Production. United Kingdon: EOLSS Publishers, 184-211.
5 Bacelar E A, Moutinho-Pereira J M, Gon?alves B C, et al. 2007. Changes in growth, gas exchange, xylem hydraulic properties and water use efficiency of three olive cultivars under contrasting water availability regimes. Environmental Experimental Botany, 60(2): 183-192.
6 Bjorksten T A, Fowler K, Pomiankowski A. 2000. What does sexual trait FA tell us about stress? Trends in Ecology and Evolution, 15(4): 163-166.
7 Blossey B, N?tzold R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5): 887-889.
8 Colautti R I, Macisaac H J, Macisaac H J. 2004. A neutral terminology to define 'invasive' species. Diversity and Distributions, 10(1): 135-141.
9 Dainese M, Leps J, de Belo F. 2015. Different effects of elevation, habitat fragmentation and grazing management on the functional, phylogenetic and taxonomic structure of mountain grasslands. Perspectives in Plant Ecology, Evolution and Systematics, 17(1): 44-53.
10 Dawson W, Moser D, van Kleunen M, et al. 2017. Global hotspots and correlates of alien species richness across taxonomic groups. Nature Ecology and Evolution, 1: 0186. doi: 10.1038/s41559-017-0186.
11 Díaz S, Kattge J, Cornelissen J H, et al. 2016. The global spectrum of plant form and function. Nature, 529(7585): 167-171.
12 Evans J R, Poorter H. 2001. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell and Environment, 24(8): 755-767.
13 Evert R F. 2013. Esau's Plant Anatomy-Meristems, Cells, and Tissues of Tree Plant Body-their Structures, Function and Development (3rd ed.). New Jersey: John Wiley & Sons, Inc., 601.
14 Fahn A. 1990. Plant Anatomy (2nd ed.). Oxford: Butterworth Heinemann, 611.
15 Falcioni R, Moriwaki T, Bonato C M, et al. 2017. Distinct growth light and gibberellin regimes alter leaf anatomy and reveal their influence on leaf optical properties. Environmental and Experimental Botany, 140(1): 86-95.
16 Gil-Pelegrín E, Saz M A, Cuadrat J M, et al.2017. Oaks under mediterranean-type climates: Functional response to summer aridity. In: Gil-Pelegrín E, Peguero-Pina, Sancho-Knapik D. Oaks Physiological Ecology. Exploring the Functional Diversity of Genus quercus L. Switzerland: Springer, 137-193.
17 Gotelli N J, Ellison A M. 2012. The analysis of multivariate. In: Gotelli N J, Ellison A M. A Primer of Ecological Statistics. Sunderland: Sinauer Associates, 383-406.
18 Hassan L M, Galal T M, Farahat E A, et al. 2015. The biology of Calotropis procera (Aiton) W.T. Trees, 29(2): 311-320.
19 Husson F, Josse J, Le S, et al. 2017. FactoMineR: multivariate exploratory data analysis and data mining. R Development Core Team. [2019-05-13]. http://factominer.free.fr/.
20 Kozlov M V, Cornelissen T, Gavrikov D E, et al. 2017. Reproducibility of fluctuating asymmetry measurements in plants: Sources of variation and implications for study design. Ecological Indicators, 73(1): 733-740.
21 Leigh A, Sevanto S, Close J D, et al. 2016. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant, Cell and Environment, 40(2): 237-248.
22 Lindorf H, Parisca L, Rodríguez P. 1991. Botanic: classification, structure and reproduction, Caracas. Venezuela: Universidad Central de Venezuela, 583. (in Spanish)
23 Mehra J. 2001. Max planck and the law of blackbody radiation. In: Mehra J. The Golden Age of Theoretical Physics. Singapore: National Academies Press, 19-55.
24 Michaletz S T, Weiser M D, Zhou J, et al. 2015. Plant thermoregulation: Energetics, trait-environment interactions, and carbon economics. Trends in Ecology and Evolution, 30(1): 714-724.
25 M?ller A P, Eriksson M. 1994. Patterns of fluctuating asymmetry in flowers: implications for sexual selection in plants. Journal of Evolutionary Biology, 7(1): 97-113.
26 Monk C D. 1966. An ecological significance of evergreenness. Ecology, 47(3): 504-505.
27 Muriira N G, Muchugi A, Yu A, et al. 2018. Genetic diversity analysis reveals genetic differentiation and strong population structure in Calotropis plants. Science Reports, 8(7832): 1-10.
28 Nagel J M, Griffin K L. 2001. Construction cost and invasive potential: comparing Lythrum salicaria (Lythraceae) with co-occurring native species along pond banks. American Journal of Botany, 88(12): 2252-2258.
29 Pagnucco K S, Maynard G A, Fera S A, et al. 2015. The future of species invasions in the Great Lakes-St. Lawrence River basin. Journal of Great Lakes Research, 41(Suppl. 1): 96-107.
30 Parkhurst D F, Loucks O L. 1972. Optimal leaf size in relation to environment. Journal of Ecology, 60(2): 505-537.
31 Parsons P A. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity, 68(4): 361-364.
32 Peguero-Pina J J, Sancho-Knapik D, Barrón E, et al. 2014. Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness. Annals of Botany, 114(1): 301-313.
33 Peguero-Pina J J, Sancho-Knapik D, Flexas J, et al. 2016a. Light acclimation of photosynthesis in two closely related firs (Abies pinsapo Boiss. and Abies alba Mill.): the role of leaf anatomy and mesophyll conductance to CO2. Tree Physiology, 36(3): 300-310.
34 Peguero-Pina J J, Sisó S, Fernández-Marín B, et al. 2016b. Leaf functional plasticity decreases the water consumption without further consequences for carbon uptake in Quercus coccifera L. under Mediterranean conditions. Tree Physiology, 36(3): 356-367.
35 Pompelli M F, Antunes W C, Ferreira D T R G, et al. 2012. Allometric models for non-destructive leaf area estimation of the Jatropha curcas. Biomass and Bioenergy, 36(1): 77-85.
36 Poorter H, Pepin S, Rijkers T, et al. 2006. Construction costs, chemical composition and payback time of high- and low-irradiance leaves. Journal of Experimental Botany, 57(2): 355-371.
37 Poorter H, Niinemets ü, Poorter L, et al. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist, 182(1): 565-588.
38 Reich P B, Walters M B, Ellsworth D S. 1992. Leaf lifespan in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs, 62(3): 365-392.
39 Rivas R, Frosi G, Ramos D G, et al. 2017. Photosynthetic limitation and mechanisms of photoprotection under drought and recovery of Calotropis procera, an evergreen C3 from arid regions. Plant Physiology and Biochemistry, 118(1): 589-599.
40 Sant'anna-Neto J L, Galvani E, Vieira B C. 2015. Climates of Brazil: past and present. In: Vieira B, Salgado A, Santos L P. Landscapes and Landforms of Brazil. World Geomorphological Landscapes. Dordrecht: Springer, 33-41.
41 Sharma B M. 1968. Root systems of some desert plants in Churu, Rajasthan. Indian Forester, 94(3): 240-246.
42 Simberloff D, Martin J-L, Genovesi P, et al. 2012. Impacts of biological invasions: what's what and the way forward. Trends in Ecology and Evolution, 28(1): 58-66.
43 Singh G. 1995. An agroforestry practice for the development of salt lands using Prosopis juliflora and Leptochloa fusca. Agroforestry Systems, 29(1): 61-75.
44 Smith H L, McAusland L, Murchie E H. 2017. Don't ignore the green light: exploring diverse roles in plant processes. Journal of Experimental Botany, 68(9): 2099-2110.
45 Souza G M, Viana J O F, Oliveira R F. 2005. Asymmetrical leaves induced by water deficit show asymmetric photosynthesis in common bean. Brazilian Journal of Plant Physiology, 17(2): 223-227.
46 Terashima I, Fujita T, Inoue T, et al. 2009. Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of qhy leaves are green. Plant and Cell Physiology, 50(4): 684-697.
47 Tezara W, Colombo R, Coronel I, et al. 2011. Water relations and photosynthetic capacity of two species of Calotropis in a tropical semi-arid ecosystem. Annals of Botany, 107(3): 397-405.
48 Thakur S, Sidhu M C. 2017. Medicinal plant remedies for dermatological problems. Current Botany, 8(1): 23-33.
49 Valladares F, Balaguer L, Martinez-Ferri E, et al. 2002. Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytologist, 156(3): 457-467.
50 Villar R, Ruiz-Robleto J, Ubera J L, et al. 2013. Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. American Journal of Botany, 100(10): 1969-1980.
51 Wang C, Zhao C Y, Xu Z, et al. 2013. Effect of vegetation on soil water retention and storage in a semi-arid alpine forest catchment. Journal of Arid Land, 5(2): 207-219.
52 Wei T, Simko V. 2016. An introduction to corrplot Package. R Development Core Team. [2019-05-13]. https://cran.r-project.org/web/packages/corrplot/vignettes/corrplot-intro.html.
53 White J W, Montes R C. 2005. Variation in parameters related to leaf thickness in common bean (Phaseolus vulgaris L.). Field Crops Research, 91(1): 7-21.
54 Witkowski E T, Lamont B B. 1991. Leaf specific mass confounds leaf density and thickness. Oecologia, 88(4): 486-493.
55 Wright I J, Reich P B, Westoby M, et al. 2004. The worldwide leaf economics spectrum. Nature, 428(6985): 821-827.
[1] Xiaobing LI, Qi HUANG, Xue MI, Yunxiao BAI, Meng ZHANG, Xu LI. Grazing every month minimizes size but boosts photosynthesis in Stipa grandis in the steppe of Inner Mongolia, China[J]. Journal of Arid Land, 2018, 10(4): 601-611.
[2] LiNa XIE, ChengCang MA, HongYu GUO, QingFang LI, YuBao GAO. Distribution pattern of Caragana species under the influence of climate gradient in the Inner Mongolia region, China[J]. Journal of Arid Land, 2014, 6(3): 311-323.
[3] Liliya A DIMEYEVA. Phytogeography of the northeastern coast of the Caspian Sea: native flora and recent colonizations[J]. Journal of Arid Land, 2013, 5(4): 439-451.
[4] Marina V OLONOVA, YuanMing ZHANG. Alien invasive species in Siberia: current status and problem[J]. Journal of Arid Land, 2013, 5(4): 428-433.
[5] Yang ZHAO, ChuanYan ZHAO, ZhongLin XU, YiYue LIU, Yao WANG, Chao WANG, HuanHua PENG, XiangLin ZHENG. Physiological responses of Populus euphratica Oliv. to groundwater table variations in the lower reaches of Heihe River, Northwest China[J]. Journal of Arid Land, 2012, 4(3): 281-291.