Sexual divergence of Populus deltoides seedlings growth and ecophysiological response to drought and rewatering

doi:10.17521/cjpe.2022.0173

Abstract

Abstract:

Aims Global climate change has aggravated the effects of drought which is one of the major factors restricting the sustainable development of agriculture and forestry. It is important to study the growth performance and the changes of physiological mechanism of dioecious plants during drought and rewatering process, which could help to understand the difference of adaptability and stress tolerance to the unfavorable environment in dioecious plants. And this paper also provides a theoretical basis for the selection of tree species for afforestation in the context of global climate change.

Methods Male and female cuttings of Populus deltoides were planted in the pots in a greenhouse, and were treated by drought stress and rewatering. The growth, leaf water parameters, and photosynthetic parameters were measured to analyze the physiological adaptability and stress tolerance of males and females under drought-rewatering conditions.

Important findings Drought stress showed negative effects on plant growth by reducing the growth of plant height and basal diameter, with decreased relative water content, water potential, net photosynthetic rate, stomatal conductance, transpiration rate, photosynthetic electron yield, photochemical quenching coefficient and electron transfer rate of leaves of males and females. There were no significant sexual differences in all parameters between males and females under sufficient water supply. Under drought stress, the growth of male plants was better than that of females, with higher growth rate of plant height and more root biomass accumulation in males. Drought resulted in the decrease of the maximum photochemical efficiency and the potential activity of photosystem II (PSII), and the increase of the intercellular CO₂ concentration of females. PSII of male plants was less damaged under drought conditions, and the photosynthetic reaction center still maintained a high light-harvesting efficiency. Meanwhile, alternating oxidase (AOX) activity was significantly increased in roots and leaves of male seedlings, which could alleviate the effect of photoinhibition. All indexes recovered after 30 days of rewatering. However, the growth rate of plant height and ground diameter, and net photosynthetic rate of males and females under drought stress were significantly lower than those of the control group without drought stress. The results showed that the growth of male and female seedlings of P. deltoides was inhibited by drought stress, and the females were more likely affected by water deficit. Water stress induced a series of adaptive physiological effects in males, including decreased leaf relative water content, decreased photosynthetic and chlorophyll fluorescence parameters, and increased activity of alternating oxidase. Therefore, males had a more effective protective mechanism than females, which was also conducive to the recovery of various functions after rewatering.

Key words: drought, rewatering, dioecious, growth physiology, Populus deltoides

SHI Meng-Jiao, LI Bin, YI Li-Ta, LIU Mei-Hua. Sexual divergence of Populus deltoides seedlings growth and ecophysiological response to drought and rewatering[J]. Chin J Plant Ecol, 2023, 47(8): 1159-1170.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2022.0173

https://www.plant-ecology.com/EN/Y2023/V47/I8/1159

Figures/Tables 7

Fig. 1 Effects of drought and re-watering on the growth of male and female seedlings of Populus deltoids (mean ± SE). FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings; TR, drought stress treatment; WR, rehydration treatment; the following number represents the processing time (d). S, sex effect; S × T, sex and treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference among treatments at the same time (p < 0.05, least-significant difference test).

Fig. 2 Effects of drought stress on biomass accumulation and allocation of Populus deltoids seedlings (mean ± SE). FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings. S, sex effect; S × T, sex and treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference among treatments at the same organ (p < 0.05, least-significant difference test).

Fig. 3 Effects of drought and re-watering on relative water content and water potential of Populus deltoids seedlings (mean ± SE). FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings. TR, drought stress treatment; WR, rehydration treatment; the following number represents the processing time (d). S, sex effect; S × T, sex and treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference among treatments at the same time (p < 0.05, least-significant difference test).

Fig. 4 Effects of drought and re-watering on the gas exchange of Populus deltoids seedlings (mean ± SE). Ci, intercellular CO2 concentration; Gs, stomatal conductance; Pn, net photosynthetic rate; Tr, transpiration rate; WUE, water use efficiency. FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings; TR, drought stress treatment; WR, rehydration treatment; the following number represents the processing time (d). S, sex effect; S × T, sex and treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference between treatments at the same time (p < 0.05, least-significant difference test).

Fig. 5 Effects of drought and re-watering on the chlorophyll fluorescence of Populus deltoids seedlings (mean ± SE). PSII, photosystem II. Fv/Fo, potential photochemical efficiency of PSII; Y(II), photosynthetic electron yield; Fv/Fm, maximal photochemical efficiency of PSII; qP, photochemical quenching; NPQ, non-photochemical quenching; ETR, electron transport rate. FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings; TR, drought stress treatment; WR, rehydration treatment; the following number represents the processing time (d). S, sex effect; S × T, sex and treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference among treatments at the same time (p < 0.05, least-significant difference test).

Fig. 6 Effects of drought and re-watering on the alternative oxidase (AOX) activity of Populus deltoids seedlings (mean ± SE). FCK, control group of female seedlings; FTR, drought treatment group of female seedlings; MCK, control group of male seedlings; MTR, drought treatment group of male seedlings. S, sex effect; S × T, sex and water treatment interaction effect; T, water treatment effect. Different lowercase letters indicate significant difference among treatments at the same time (p < 0.05, least-significant difference test).

Fig. 7 Correlation coefficients of photosynthetic variables, chlorophyll fluorescence and alternative oxidase (AOX) activity of male (A) and female (B) Populus deltoids seedlings. Data are Pearson correlation coefficients. *, p < 0.05; **, p < 0.01. Ci, intercellular CO2 concentration; ETR, electron transport rate; Fv/Fm, maximal photochemical efficiency of PSII; Fv/Fo, potential photochemical efficiency of PSII; Gs, stomatal conductance; L, leaf; NPQ, non-photochemical quenching; Pn, net photosynthetic rate; PSII, photosystem II; qP, photochemical quenching; R, root; S, stem; Tr, transpiration rate; WUE, water use efficiency; Y(II), photosynthetic electron yield.

References 48

[1]	Ali S, Hayat K, Iqbal A, Xie LN (2020). Implications of abscisic acid in the drought stress tolerance of plants. Agronomy, 10, 1323. DOI: 10.3390/agronomy10091323.
[2]	Bartoli CG, Gomez F, Gergoff G, Guiamét JJ, Puntarulo S (2005). Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. Journal of Experimental Botany, 56, 1269-1276. DOI PMID
[3]	Baurain D, Dinant M, Coosemans N, Matagne RF (2003). Regulation of the alternative oxidase Aox1 gene in Chlamydomonas reinhardtii. Role of the nitrogen source on the expression of a reporter gene under the control of the Aox1 promoter. Plant Physiology, 131, 1418-1430. PMID
[4]	Chastain DR, Snider JL, Collins GD, Perry CD, Whitaker J, Byrd SA (2014). Water deficit in field-grown Gossypium hirsutum primarily limits net photosynthesis by decreasing stomatal conductance, increasing photorespiration, and increasing the ratio of dark respiration to gross photosynthesis. Journal of Plant Physiology, 171, 1576-1585. DOI PMID
[5]	Chen J, Dong TF, Duan BL, Korpelainen H, Niinemets Ü, Li CY (2015). Sexual competition and N supply interactively affect the dimorphism and competiveness of opposite sexes in Populus cathayana. Plant, Cell & Environment, 38, 1285-1298.
[6]	Chen J, Duan BL, Wang ML, Korpelainen H, Li CY (2014). Intra- and inter-sexual competition of Populus cathayana under different watering regimes. Functional Ecology, 28, 124-136. DOI URL
[7]	Chen LH (2011). Differences of Physiological and Ecological Responses of Male and Female Plants of Populus yunnanensis to Environmental Stress. PhD dissertation, University of Chinese Academy of Sciences, Beijing.
	[陈良华 (2011). 滇杨(Populus yunnanensis)雌雄植株对环境胁迫的生理生态响应差异. 博士学位论文, 中国科学院大学, 北京.]
[8]	Dahal K, Vanlerberghe GC (2017). Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought. New Phytologist, 213, 560-571. DOI PMID
[9]	Duan QY, Tian Y, E XW, Qin GZ, Zhang JY (2020). Sexual differences in growth and physiological properties of southern-type poplar clones in response to continuous drought and re-watering. Chinese Journal of Ecology, 39, 2140-2150.
	[段启英, 田野, 鄂晓伟, 秦广震, 张贾宇 (2020). 南方型黑杨生长和生理特性对持续干旱和复水响应的性别差异. 生态学杂志, 39, 2140-2150.]
[10]	Efeoğlu B, Ekmekçi Y, Çiçek N (2009). Physiological responses of three maize cultivars to drought stress and recovery. South African Journal of Botany, 75, 34-42. DOI URL
[11]	Fang YJ, Xiong LZ (2015). General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences, 72, 673-689. DOI PMID
[12]	Finnegan PM, Umbach AL, Wilce JA (2003). Prokaryotic origins for the mitochondrial alternative oxidase and plastid terminal oxidase nuclear genes. FEBS Letters, 555, 425-430. PMID
[13]	Fu YY (2018). Stomatal and non-stomatal limitation of photosynthesis in plant leaves under water stress. Science and Technology & Innovation, (8), 57-58.
	[符玉英 (2018). 水分胁迫下植物叶片光合的气孔和非气孔限制. 科技与创新, (8), 57-58.]
[14]	Galvez DA, Landhäusser SM, Tyree MT (2011). Root carbon reserve dynamics in aspen seedlings: Does simulated drought induce reserve limitation? Tree Physiology, 31, 250-257. DOI PMID
[15]	Gao TH, Shang JZ, Song LT, Wang WF (2021). Responses of leaf photosynthetic and anatomical characteristics in Populus simonii cuttings to drought and re-watering. Science of Soil and Water Conservation, 19(6), 18-26.
	[高钿惠, 尚佳州, 宋立婷, 王卫锋 (2021). 小叶杨叶片光合特性与解剖结构对干旱及复水的响应. 中国水土保持科学, 19(6), 18-26.]
[16]	Hultine KR, Grady KC, Wood TE, Shuster SM, Stella JC, Whitham TG (2016). Climate change perils for dioecious plant species. Nature Plants, 2, 16109. DOI: 10.1038/nplants.2016.109. PMID
[17]	Jing X, Wang JD, Wang JH, Huang WJ, Liu LY (2008). Classifying forest vegetation using sub-region classification based on multi-temporal remote sensing images. Remote Sensing Technology and Application, 23, 394-397.
	[竞霞, 王锦地, 王纪华, 黄文江, 刘良云 (2008). 基于分区和多时相遥感数据的山区植被分类研究. 遥感技术与应用, 23, 394-397.]
[18]	Lei YB, Yin CY, Li CY (2006). Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiologia Plantarum, 127, 182-191. DOI URL
[19]	Leigh A, Nicotra AB (2003). Sexual dimorphism in reproductive allocation and water use efficiency in Maireana pyramidata (Chenopodiaceae), a dioecious, semi-arid shrub. Australian Journal of Botany, 51, 509-514. DOI URL
[20]	Li CY, Yin CY, Liu SR (2004). Different responses of two contrasting Populus davidiana populations to exogenous abscisic acid application. Environmental and Experimental Botany, 51, 237-246. DOI URL
[21]	Li JW, Wang JX, Zhang ML, Ji ZB, Xue S (2009). Effect of drought and rewater on leaf water potential of Robinia pseudoacacia. Journal of Northwest Forestry University, 24(3), 33-36.
	[李继文, 王进鑫, 张慕黎, 吉增宝, 薛设 (2009). 干旱及复水对刺槐叶水势的影响. 西北林学院学报, 24(3), 33-36.]
[22]	Li L, Li XY, Lin LS, Wang YJ, Xue W (2011). Photosystem II characteristics of nine Gramineae species in southern Taklamakan Desert. Chinese Journal of Applied Ecology, 22, 2599-2603.
	[李磊, 李向义, 林丽莎, 王迎菊, 薛伟 (2011). 塔克拉玛干沙漠南缘9种禾本科牧草光系统II特性. 应用生态学报, 22, 2599-2603.]
[23]	Liao T, Wang Y, Xu CP, Li Y, Kang XY (2018). Adaptive photosynthetic and physiological responses to drought and rewatering in triploid Populus populations. Photosynthetica, 56, 578-590. DOI URL
[24]	Limousin JM, Bickford CP, Dickman LT, Pangle RE, Hudson PJ, Boutz AL, Gehres N, Osuna JL, Pockman WT, McDowell NG (2013). Regulation and acclimation of leaf gas exchange in a piñon-juniper woodland exposed to three different precipitation regimes. Plant, Cell & Environment, 36, 1812-1825.
[25]	Liu CG, Wang YJ, Pan KW, Wang QW, Liang J, Jin YQ, Tariq A (2017). The synergistic responses of different photoprotective pathways in dwarf bamboo (Fargesia rufa) to drought and subsequent rewatering. Frontiers in Plant Science, 8, 489. DOI: 10.3389/fpls.2017.00489.
[26]	Liu KQ, Liu WH, Jia ZF, Ma X, Liang GL (2020). Effects of water stress on organ growth and water use efficiency of Avena sativa ‘Qingyan No. 1’. Acta Agrestia Sinica, 28, 1552-1562.
	[刘凯强, 刘文辉, 贾志锋, 马祥, 梁国玲 (2020). 干旱胁迫对‘青燕1号’燕麦器官生长及水分利用效率的影响. 草地学报, 28, 1552-1562.] DOI
[27]	Liu M, Zhao Y, Wang YT, Korpelainen H, Li CY (2022). Stem xylem traits and wood formation affect sex-specific responses to drought and rewatering in Populus cathayana. Tree Physiology, 42, 1350-1363. DOI URL
[28]	Mathobo R, Marais D, Steyn JM (2017). The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.). Agricultural Water Management, 180, 118-125. DOI URL
[29]	Mu Q, Dong MQ, Xu J, Cao YX, Ding YB, Sun SK, Cai HJ (2022). Photosynthesis of winter wheat effectively reflected multiple physiological responses under short-term drought-rewatering conditions. Journal of the Science of Food and Agriculture, 102, 2472-2483. DOI URL
[30]	Nakamura K, Sakamoto K, Kido Y, Fujimoto Y, Suzuki T, Suzuki M, Yabu Y, Ohta N, Tsuda A, Onuma M, Kita K (2005). Mutational analysis of the Trypanosoma vivax alternative oxidase: the E(X)₆Y motif is conserved in both mitochondrial alternative oxidase and plastid terminal oxidase and is indispensable for enzyme activity. Biochemical and Biophysical Research Communications, 334, 593-600. DOI PMID
[31]	Ni SL, Li XM, Wang YC, Ren GS (2018). Physiological development and water use efficiency of winter wheat after re-watering following drought stresses at different growth stages. Journal of Irrigation and Drainage, 37(11), 20-25.
	[倪胜利, 李兴茂, 王亚翠, 任根深 (2018). 旱后复水对冬小麦生长发育及水分利用效率的影响. 灌溉排水学报, 37(11), 20-25.]
[32]	Peng SM, Jiang H, Zhang S, Chen LH, Li XG, Korpelainen H, Li CY (2012). Transcriptional profiling reveals sexual differences of the leaf transcriptomes in response to drought stress in Populus yunnanensis. Tree Physiology, 32, 1541-1555. DOI URL
[33]	Renner SS (2014). The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany, 101, 1588-1596. DOI PMID
[34]	Rubin RL, van Groenigen KJ, Hungate BA (2017). Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant and Soil, 416, 309-323. DOI URL
[35]	Song XY, Zhou GS, He QJ (2021). Critical leaf water content for maize photosynthesis under drought stress and its response to rewatering. Sustainability, 13, 7218. DOI: 10.3390/su13137218.
[36]	Tardieu F, Tuberosa R (2010). Dissection and modelling of abiotic stress tolerance in plants. Current Opinion in Plant Biology, 13, 206-212. DOI PMID
[37]	Tian K, Wang Y, Chen D, Cao M, Luo J (2022). Influence of drought stress and post-drought rewatering on phytoremediation effect of Arabidopsis thaliana. Bulletin of Environmental Contamination and Toxicology, 108, 594-599. DOI
[38]	Wang J, Vanlerberghe GC (2013). A lack of mitochondrial alternative oxidase compromises capacity to recover from severe drought stress. Physiologia Plantarum, 149, 461-473. DOI URL
[39]	Wang YL, Sun JW, Xun SH, Zang DK, Fang XX, Zhang T (2017). Effects of drought stress on photosynthetic characteristics, fluorescence parameters and relative water content of ‘Dong Yue Hong’ leaves. Shandong Agricultural Sciences, 49(4), 46-50.
	[王玉丽, 孙居文, 荀守华, 臧德奎, 方晓晓, 张涛 (2017). 干旱胁迫对东岳红光合特性、叶绿素荧光参数及叶片相对含水量的影响. 山东农业科学, 49(4), 46-50.]
[40]	Xu X, Yang F, Xiao XW, Zhang S, Korpelainen H, Li CY (2008). Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant, Cell & Environment, 31, 850-860.
[41]	Xu XY, Sun S, Jin LQ, Liu MJ, Gao HY (2015). Up-regulation of the mitochondrial alternative oxidase pathway enhances photoprotection in Malus hupehensis leaves under drought stress. Plant Physiology Journal, 51, 2119-2125.
	[徐秀玉, 孙山, 金立桥, 刘美君, 高辉远 (2015). 干旱胁迫下平邑甜茶叶片交替呼吸途径上调对光破坏的防御作用. 植物生理学报, 51, 2119-2125.]
[42]	Yang B, Liu ZZ, Peng FR, Cao F, Chen T, Deng QJ, Chen WJ (2017). Growth and photosynthetic characteristics for pecan cultivars during drought stress and recovery. Journal of Zhejiang A&F University, 34, 991-998.
	[杨标, 刘壮壮, 彭方仁, 曹凡, 陈涛, 邓秋菊, 陈文静 (2017). 干旱胁迫和复水下不同薄壳山核桃品种的生长和光合特性. 浙江农林大学学报, 34, 991-998.]
[43]	Yu SY, Zhou YF, Huang W, Wang X, Gao XQ, Fu BZ (2021). Effects of drought, salt, and drought-salt combined stress on photosynthetic and physiological characteristics of Agropyron mongolicum. Acta Agrestia Sinica, 29, 2399-2406.
	[余淑艳, 周燕飞, 黄薇, 王星, 高雪芹, 伏兵哲 (2021). 干旱、盐及旱盐复合胁迫对沙芦草光合和生理特性的影响. 草地学报, 29, 2399-2406.] DOI
[44]	Zhang S, Chen FG, Peng SM, Ma WJ, Korpelainen H, Li CY (2010). Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress. Proteomics, 10, 2661-2677. DOI URL
[45]	Zhang S, Chen LH, Duan BL, Korpelainen H, Li CY (2012). Populus cathayana males exhibit more efficient protective mechanisms than females under drought stress. Forest Ecology and Management, 275, 68-78. DOI URL
[46]	Zhang ZH, Cao BL, Gao S, Xu K (2019). Grafting improves tomato drought tolerance through enhancing photosynthetic capacity and reducing ROS accumulation. Protoplasma, 256, 1013-1024. DOI PMID
[47]	Zhao WH, Liu LZ, Shen Q, Yang JH, Han XY, Tian F, Wu JJ (2020). Effects of water stress on photosynthesis, yield, and water use efficiency in winter wheat. Water, 12, 2127. DOI: 10.3390/w12082127.
[48]	Zhao YQ, Gao MQ, Li T, Wang WF (2020). Effects of water stress on leaf gas exchange and biomass allocation of Populus × popularis ‘35-44’ cuttings. Acta Ecologica Sinica, 40, 1683-1689.
	[赵瑜琦, 高苗琴, 李涛, 王卫锋 (2020). 干旱胁迫对群众杨光合特性与器官干物质分配的影响. 生态学报, 40, 1683-1689.]