Effects of provenance on leaf structure and function of two mangrove species: the genetic adaptation to temperature

doi:10.17521/cjpe.2021.0221

Abstract

Abstract:

Aims Plant leaves have the ability to adjust phenotypic characteristics according to different environmental conditions. The adaptability of leaf traits to the environment directly affects the survival, distribution and migration of plants under climate change. With global warming, mangrove forests have been expanding to higher latitudes. However, there is still a lack of understanding about the genetic adaptation of leaf traits of different mangrove species to temperature variation of native habitats.
Methods The leaf anatomical structure and physiological function parameters of the seedlings from 6 provenances of Bruguiera gymnorhiza and 5 provenances of Kandelia obovata were measured, which were grown in a common garden. The relationships between the leaf anatomical traits and physiological function of mangrove seedlings were analyzed, and the genetic adaptation of two mangrove species to the temperature of provenance was analyzed.
Important findings The leaf thickness, thickness of palisade tissue, cuticle and epidermis of B. gymnorhiza seedlings were significantly negatively correlated with the mean annual temperature of their native habitats. Compared with the seedlings of B. gymnorhiza, the K. obovata seedlings had thicker leaf epidermis and cuticle, and the anatomical traits of K. obovata were not correlated with the annual average temperature of the provenances. Pooling the data of the seedlings of different provenances of the two species together, the palisade tissue and to a lesser extend spongy tissue were positively correlated with photosynthetic rate, suggesting an important role of palisade tissue for photosynthesis in mangroves. There was also a significant positive correlation between vein density and stomatal density, maximum stomatal conductance, revealing genetic adaptation for the balance between leaf transpirational demand and water supply. In conclusion, B. gymnorhiza showed the significant genetic adaptation to the temperature of the provenance, while K. obovata did not. The leaf anatomical structure of K. obovata adapts to the temperature of provenance through the persistent inheritance of stress resistance of leaf structure. The differences of leaf structure lead to the corresponding changes of physiological functions such as photosynthesis and maximum stomatal conductance of mangroves, which is conducive to the survival and reproduction of mangroves under the climate change.

Key words: provenance, mangrove, leaf anatomy, photosynthetic characteristics, temperature

ZHANG Xiao-Yan, WEE Kim Shan Alison, KAJITA Tadashi, CAO Kun-Fang. Effects of provenance on leaf structure and function of two mangrove species: the genetic adaptation to temperature[J]. Chin J Plant Ecol, 2021, 45(11): 1241-1250.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0221

https://www.plant-ecology.com/EN/Y2021/V45/I11/1241

Figures/Tables 6

Table 1 Geographical location and mean annual temperature of the selected provenances of two mangrove species in this study

树种 Species	种源地 Provenance	地理坐标 Geographical coordinates	年平均气温 Mean annual temperature (℃)
木榄 Bruguiera gymnorhiza	中国文昌 Wenchang, China	19.62° N, 110.84° E	24.4
	中国北海 Beihai, China	21.50° N, 109.76° E	23.2
	中国福田 Futian, China	22.52° N, 114.01° E	22.6
	中国云霄 Yunxiao, China	23.86° N, 117.51° E	21.0
	日本西田川 Nishida, Japan	24.41° N, 123.78° E	23.0
	日本冲绳 Okinawa, Japan	26.66° N, 128.01° E	21.9
秋茄树 Kandelia obovata	中国山口 Shankou, China	21.42° N, 109.21° E	23.2
	中国云霄 Yunxiao, China	23.92° N, 117.42° E	20.7
	日本西田川 Nishida, Japan	24.39° N, 123.82° E	23.0
	日本冲绳 Okinawa, Japan	26.46° N, 127.94° E	22.3
	中国福鼎 Fuding, China	27.28° N, 120.30° E	18.4

Fig. 1 Comparison of leaf structural composition of Bruguiera gymnorhiza (A) and Kandelia obovata (B) from different provenances.

Fig. 2 Correlation between leaf anatomical structure of Bruguiera gymnorhiza and Kandelia obovata seedlings from different provenances and mean annual temperature of native habitats. R1, p1 represents the seedlings of Bruguiera gymnorhiza; R2, p2 represents the seedlings of Kandelia obovata.

Fig. 3 Correlation between leaf vein density and stomatal density (A), maximum stomatal conductance (B) and palisade tissue thickness (C) of seedlings of Bruguiera gymnorhiza and Kandelia obovata from different provenances (mean ± SE).

Fig. 4 Correlation between photosynthetic rate and spongy tissue thickness (A), palisade tissue thickness (B), vein density (C) and leaf thickness (D) of seedlings of Bruguiera gymnorhiza and Kandelia obovata from different provenances (mean ± SE).

Fig. 5 Principal component analysis of 8 leaf anatomical structure characters (A) and 11 provenances (B) of Bruguiera gymnorhiza and Kandelia obovata seedlings from different provenances. CT, cuticle thickness; LT, leaf thickness; Pn, photosynthetic rate; PT, palisade tissue thickness; RPS, palisade tissue thickness/spongy tissue thickness; SD, stomatal density; ST, sponge tissue thickness; VD, vein density.

References 37

[1]	Alberto FJ, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F, Lenormand T, Yeaman S, Whetten R, Savolainen O (2013). Potential for evolutionary responses to climate change—Evidence from tree populations. Global Change Biology, 19, 1645-1661. DOI URL
[2]	Brodersen CR, Vogelmann TC (2007). Do epidermal lens cells facilitate the absorptance of diffuse light? American Journal of Botany, 94, 1061-1066. DOI PMID
[3]	Brodribb TJ, Jordan GJ (2011). Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist, 192, 437-448. DOI PMID
[4]	Burrows MT, Schoeman DS, Richardson AJ, Molinos JG, Hoffmann A, Buckley LB, Moore PJ, Brown CJ, Bruno JF, Duarte CM, Halpern BS, Hoegh-Guldberg O, Kappel CV, Kiessling W, O’Connor MI, et al. (2014). Geographical limits to species-range shifts are suggested by climate velocity. Nature, 507, 492-495. DOI URL
[5]	Caringella MA, Bongers FJ, Sack L (2015). Leaf hydraulic conductance varies with vein anatomy across Arabidopsis thaliana wild-type and leaf vein mutants. Plant, Cell & Environment, 38, 2735-2746.
[6]	Chen BY, Wang CH, Tian YK, Chu QG, Hu CH (2015). Anatomical characteristics of young stems and mature leaves of dwarf pear. Scientia Horticulturae, 186, 172-179. DOI URL
[7]	Chen Y, Liu KD, Li HL, Xu FH, Zhong JD, Cheng XL, Yuan CC (2014). Leaf structures and stress resistance in five mangrove species. Journal of Northeast Forestry University, 42(7), 27-31.
	[ 陈燕, 刘锴栋, 黎海利, 许方宏, 钟军弟, 成夏岚, 袁长春 (2014). 5种红树植物的叶片结构及其抗逆性比较. 东北林业大学学报, 42(7), 27-31.]
[8]	Corlett RT, Westcott DA (2013). Will plant movements keep up with climate change? Trends in Ecology & Evolution, 28, 482-488. DOI URL
[9]	DeLucia EH, Nelson K, Vogelmann TC, Smith WK (1996). Contribution of intercellular reflectance to photosynthesis in shade leaves. Plant, Cell & Environment, 19, 159-170.
[10]	Domínguez E, Cuartero J, Heredia A (2011). An overview on plant cuticle biomechanics. Plant Science, 181, 77-84. DOI PMID
[11]	Drake JE, Aspinwall MJ, Pfautsch S, Rymer PD, Reich PB, Smith RA, Crous KY, Tissue DT, Ghannoum O, Tjoelker MG (2015). The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Global Change Biology, 21, 459-472. DOI PMID
[12]	Ellison JC, Stoddart DR (1991). Mangrove ecosystem collapse during predicted sea-level rise: holocene analogues and implications. Journal of Coastal Research, 7, 151-165.
[13]	González-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N, Laffan SW, Miller JT, Rosauer DF, Faith DP, Nipperess DA, Kujala H, Linke S, Butt N, Külheim C, Crisp MD, Gruber B (2016). Phylogenetic approaches reveal biodiversity threats under climate change. Nature Climate Change, 6, 1110-1114. DOI
[14]	Gorsuch PA, Pandey S, Atkin OK (2010). Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves. Plant, Cell & Environment, 33, 244-258.
[15]	Han XB, Li RQ, Wang JB (1997). Cellular structural comparison between different thermo-resistant cultivars of Raphanus sativus L. under heat stress. Journal of Wuhan Botanical Research, 15, 173-178.
	[ 韩笑冰, 利容千, 王建波 (1997). 热胁迫下萝卜不同耐热性品种细胞组织结构比较. 武汉植物学研究, 15, 173-178.]
[16]	Hanba YT, Miyazawa SI, Terashima I (1999). The influence of leaf thickness on the CO₂ transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology, 13, 632-639. DOI URL
[17]	Ji RX, Yu X, Chang Y, Shen C, Bai XK, Xia XL, Yin WL, Liu C (2020). Geographical provenance variation of leaf anatomical structure of Caryopteris mongholica and its significance in response to environmental changes. Chinese Journal of Plant Ecology, 44, 277-286. DOI URL
	[ 纪若璇, 于笑, 常远, 沈超, 白雪卡, 夏新莉, 尹伟伦, 刘超 (2020). 蒙古莸叶片解剖结构的地理种源变异及其对环境变化响应的意义. 植物生态学报, 44, 277-286.]
[18]	Ji ZJ, Quan XK, Wang CK (2013). Variations in leaf anatomy of Larix gmelinii reflect adaptation of its photosynthetic capacity to climate changes. Acta Ecologica Sinica, 33, 6967-6974. DOI URL
	[ 季子敬, 全先奎, 王传宽 (2013). 兴安落叶松针叶解剖结构变化及其光合能力对气候变化的适应性. 生态学报, 33, 6967-6974.]
[19]	Kröber W, Heklau H, Bruelheide H (2015). Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits. Plant Biology, 17, 373-383. DOI PMID
[20]	Li YY, Lin P (2006). Anatomical characteristics of leaves in three mangrove species. Journal of Tropical and Subtropical Botany, 14, 301-306.
	[ 李元跃, 林鹏 (2006). 三种红树植物叶片的比较解剖学研究. 热带亚热带植物学报, 14, 301-306.]
[21]	Liao BW, Zhang QM (2014). Area, distribution and species composition of mangroves in China. Wetland Science, 12, 435-440.
	[ 廖宝文, 张乔民 (2014). 中国红树林的分布、面积和树种组成. 湿地科学, 12, 435-440.]
[22]	Ma XF, Wang XF, Li Q, He X (2013). The analysis of drought resistance and the comparison of anatomical structures of the leave of Xanthoceras sorbifolia Bunge introduced from different regions. Journal of Arid Land Resources and Environment, 27, 92-96.
	[ 马小芬, 王兴芳, 李强, 贺晓 (2013). 不同种源地文冠果叶片解剖结构比较及抗旱性分析. 干旱区资源与环境, 27, 92-96.]
[23]	McCann S, Greenlees MJ, Newell D, Shine R (2014). Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range. Functional Ecology, 28, 1166-1174. DOI URL
[24]	Méndez-Alonzo R, López-Portillo J, Rivera-Monroy VH (2008). Latitudinal variation in leaf and tree traits of the mangrove Avicennia germinans (Avicenniaceae) in the central region of the Gulf of Mexico. Biotropica, 40, 449-456. DOI URL
[25]	Miao C, Li RQ, Wang JB (1994). Leaf structural changes of Brassica campestris and B. oleracea in response to heat stress. Journal of Wuhan Botanical Research, 12, 207-211.
	[ 苗琛, 利容千, 王建波 (1994). 热胁迫下不结球白菜和甘蓝叶片组织结构的变化. 武汉植物学研究, 12, 207-211.]
[26]	Oguchi R, Hikosaka K, Hirose T (2005). Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell & Environment, 28, 916-927.
[27]	Parkhurst DF (1994). Diffusion of CO₂ and other gases inside leaves. New Phytologist, 126, 449-479. DOI PMID
[28]	Poulson ME, Vogelmann TC (1990). Epidermal focussing and effects upon photosynthetic light-harvesting in leaves of Oxalis. Plant, Cell & Environment, 13, 803-811.
[29]	Rueden CT, Hiner MC, Eliceiri KW (2016). ImageJ: image analysis interoperability for the next generation of biological image data. Microscopy and Microanalysis, 22, 2066-2067. DOI URL
[30]	Suarez AV, Tsutsui ND (2008). The evolutionary consequences of biological invasions. Molecular Ecology, 17, 351-360. DOI URL
[31]	Tian SQ, Zhu SD, Zhu JJ, Shen ZH, Cao KF (2016). Impact of leaf morphological and anatomical traits on mesophyll conductance and leaf hydraulic conductance in mangrove plants. Plant Science Journal, 34, 909-919.
	[ 田尚青, 朱师丹, 朱俊杰, 申智骅, 曹坤芳 (2016). 红树林植物叶片形态和解剖特征对叶肉导度、叶片导水率的影响. 植物科学学报, 34, 909-919.]
[32]	Vogelmann TC, Martin G (1993). The functional significance of palisade tissue: penetration of directional versus diffuse light. Plant, Cell & Environment, 16, 65-72.
[33]	Vogelman TC, Nishio JN, Smith WK (1996). Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends in Plant Science, 1, 65-70. DOI URL
[34]	Wen Y, Zhao WL, Cao KF (2020). Global convergence in the balance between leaf water supply and demand across vascular land plants. Functional Plant Biology, 47, 904-911. DOI URL
[35]	Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, et al. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827. DOI URL
[36]	Xiong DL, Flexas J, Yu TT, Peng SB, Huang JL (2017). Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO₂ in Oryza. New Phytologist, 213, 572-583. DOI URL
[37]	Zheng JJ, Lu W, Chen LH, Li PC (1996). Relationship between leaf rate of leaf air space in longan and Chinese olive and cold resistance. Journal of Fujian Agricultural University, 25(2), 40-43.
	[ 郑家基, 卢炜, 陈利恒, 李平聪 (1996). 龙眼、橄榄叶片空隙率与耐寒性的关系. 福建农业大学学报, 25(2), 40-43.]