Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

doi:10.1016/j.pld.2020.11.007

Plant Diversity ›› 2021, Vol. 43 ›› Issue (04): 324-330.DOI: 10.1016/j.pld.2020.11.007

Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

Feng-Ping Zhang^a,b,c, Jiao-Lin Zhang^a, Timothy J. Brodribb^d, Hong Hu^c

a CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
b College of Traditional Chinese Medicine, Yunnan Key Laboratory of Dai and Yi Medicines, Yunnan University of Chinese Medicine, Kunming, 650500, Yunnan, China;
c Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, Yunnan Key Laboratory for Wild Plant Resources, Kunming 650201, Yunnan, China;
d School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia

收稿日期:2020-07-05 修回日期:2020-11-04 出版日期:2021-08-25 发布日期:2021-09-07
通讯作者: Jiao-Lin Zhang
基金资助:
We thank Rong-Fei Chen and Jing-Qiu Feng for assistance with measurements of anatomical traits and water potentials. We thank Zhi-Jia Gu for providing technical support with electron microscopy. This study was supported by the National Natural Science Foundation of China (31670415, 31870385, 31960224), the "Young Top Talents" Ten Thousands Plan in Yunnan Province (YNWR-QNBJ-2018-337), Science research of Yunnan Provincial Department of Education (2019J1068) and open funding from the CAS Key Laboratory of Tropical Forest Ecology to F.P. Zhang.

Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

Feng-Ping Zhang^a,b,c, Jiao-Lin Zhang^a, Timothy J. Brodribb^d, Hong Hu^c

a CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
b College of Traditional Chinese Medicine, Yunnan Key Laboratory of Dai and Yi Medicines, Yunnan University of Chinese Medicine, Kunming, 650500, Yunnan, China;
c Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, Yunnan Key Laboratory for Wild Plant Resources, Kunming 650201, Yunnan, China;
d School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia

Received:2020-07-05 Revised:2020-11-04 Online:2021-08-25 Published:2021-09-07
Contact: Jiao-Lin Zhang
Supported by:
We thank Rong-Fei Chen and Jing-Qiu Feng for assistance with measurements of anatomical traits and water potentials. We thank Zhi-Jia Gu for providing technical support with electron microscopy. This study was supported by the National Natural Science Foundation of China (31670415, 31870385, 31960224), the "Young Top Talents" Ten Thousands Plan in Yunnan Province (YNWR-QNBJ-2018-337), Science research of Yunnan Provincial Department of Education (2019J1068) and open funding from the CAS Key Laboratory of Tropical Forest Ecology to F.P. Zhang.

摘要/Abstract

摘要： Variation in resistance of xylem to embolism among flowers, leaves, and stems strongly influences the survival and reproduction of plants. However, little is known about the vulnerability to xylem embolism under drought stress and their relationships to the anatomical traits of pits among reproductive and vegetative organs. In this study, we investigated the variation in xylem vulnerability to embolism in peduncles, petioles, and stems in a woody plant, Magnolia grandiflora. We analyzed the relationships between water potentials that induced 50% embolism (P₅₀) in peduncles, petioles, and stems and the conduit pit traits hypothesized to influence cavitation resistance. We found that peduncles were more vulnerable to cavitation than petioles and stems, supporting the hypothesis of hydraulic vulnerability segmentation that leaves and stems are prioritized over flowers during drought stress. Moreover, P₅₀ was significantly correlated with variation in the dimensions of inter-vessel pit apertures among peduncles, petioles and stems. These findings highlight that measuring xylem vulnerability to embolism in reproductive organs is essential for understanding the effect of drought on plant reproductive success and mortality under drought stress.

关键词: Drought, Flower, Pit traits, Xylem embolism, Magnolia

Abstract: Variation in resistance of xylem to embolism among flowers, leaves, and stems strongly influences the survival and reproduction of plants. However, little is known about the vulnerability to xylem embolism under drought stress and their relationships to the anatomical traits of pits among reproductive and vegetative organs. In this study, we investigated the variation in xylem vulnerability to embolism in peduncles, petioles, and stems in a woody plant, Magnolia grandiflora. We analyzed the relationships between water potentials that induced 50% embolism (P₅₀) in peduncles, petioles, and stems and the conduit pit traits hypothesized to influence cavitation resistance. We found that peduncles were more vulnerable to cavitation than petioles and stems, supporting the hypothesis of hydraulic vulnerability segmentation that leaves and stems are prioritized over flowers during drought stress. Moreover, P₅₀ was significantly correlated with variation in the dimensions of inter-vessel pit apertures among peduncles, petioles and stems. These findings highlight that measuring xylem vulnerability to embolism in reproductive organs is essential for understanding the effect of drought on plant reproductive success and mortality under drought stress.

Key words: Drought, Flower, Pit traits, Xylem embolism, Magnolia

Feng-Ping Zhang, Jiao-Lin Zhang, Timothy J. Brodribb, Hong Hu. Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora[J]. Plant Diversity, 2021, 43(04): 324-330.

参考文献

Adams, H.D., Zeppel, M.J.B., Anderegg, W.R.L., et al., 2017. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat. Ecol. Evol. 1, 1285-1291.
Anderegg, W.R.L., Klein, T., Bartlett, M., et al., 2016. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl. Acad. Sci. U.S.A. 113, 5024-5029.
Barigah, T.S., Charrier, O., Douris, M., et al., 2013. Water stress-induced xylem hydraulic failure is a causal factor of tree mortality in beech and poplar. Ann. Bot. 112, 1431-1437.
Blackman, C.J., Brodribb, T.M., Jordan, G.J., 2010. Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol. 188, 1113-1123.
Bouche, P.S., Larter, M., Domec, J.C., et al., 2014. A broad survey of hydraulic and mechanical safety in the xylem of conifers. J. Exp. Bot. 65, 4419-4431.
Bourbia, I., Carins-Murphy, M.R., Gracie, A., et al., 2020. Xylem cavitation isolates leaky flowers during water stress in pyrethrum. New Phytol. 227, 146-155.
Bréda, N., Huc, R., Granier, A., et al., 2006. Temperate forest trees and stands under severe drought:a review of ecophysiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 63, 625-644.
Brodribb, T.J., Cochard, H., 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575-584.
Brodribb, T.J., Bowman, D.J.M.S., Nichols, S., et al., 2010. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol. 188, 533-542.
Brodribb, T.J., Skelton, R.P., McAdam, S.A.M., et al., 2016. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure, New Phytol. 209, 1403-1409.
Brodribb, T.J., Carriqui, M., Delzon, S., et al., 2017. Optical measurement of stem xylem vulnerability. Plant Physiol. 174, 2054-2061.
Brodribb, T.J., Powers, J., Cochard, H., et al., 2020. Hanging by a thread? Forests and drought. Science 368, 261-266.
Boyer, I.S., Westgate., M.E., 2004. Grain yields with limited water. J. Exp. Bot. 55, 2385-2394.
Chen, Y.J., Maenpuen, P., Zhang, Y.J., et al., 2020. Quantifying vulnerability to embolism in tropical trees and lianas using five methods:Can discrepancies be explained by xylem structural traits? New Phytol. https://doi.org/10.1111/nph.16927.
Choat, B., Ball, M.C., Luly, J.G., et al., 2005. Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees 19, 305-311.
Choat, B., Cobb, A.R., Jansen, S., 2008. Structure and function of bordered pits:new discoveries and impacts on whole-plant hydraulic function. New Phytol. 177, 608-626.
Choat, B., Jansen, S., Brodribb, T.J., et al., 2012. Global convergence in the vulnerability of forests to drought. Nature 491, 752-755.
Feild, T.S., Chatelet, D.S., Brodribb, T.J., 2009. Giant flowers of Southern magnolia are hydrated by the xylem. Plant Physiol. 150, 1587-1597.
Hacke, U.G., Jacobsen, A.L., Pratt, R.B., 2009. Xylem function of arid-land shrubs from California, USA:an ecological and evolutionary analysis. Plant Cell Environ. 32, 1324-1333.
Hargrave, K.R., Kolb, K.J., Ewers, F.W., et al., 1994. Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol. 126, 695-705.
Hochberg, U., Windt, C.W., Ponomarenko, A., et al., 2017. Stomatal closure, basal leaf embolism and shedding protect the hydraulic integrity of grape stems. Plant Physiol. 174, 764-775.
Jansen, S., Choat, B., Pletsers, A., 2009. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am. J. Bot. 96, 409-419.
Johnson, D.M., McCulloh, K.A., Meinzer, F.C., et al., 2011. Hydraulic patterns and safety margins, from stem to stomata, in three eastern U.S. tree species. Tree Physiol. 31, 659-668.
Lambrecht, S.C., 2013. Floral water costs and size variation in the highly selfing Leptosiphon bicolor (Polemoniaceae). Int. J. Plant Sci. 174, 74-84.
Lens, F., Sperry, J.S., Christman, M.A., et al., 2011. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol. 190, 209-723.
Li, S., Lens, F., Espino, S., et al., 2016. Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J. 37, 152-171.
Memmott, J., Waser, N.M., 2002. Integration of alien plants into a native flower-pollinator visitation web. Proc. Roy. Soc. B Biol. Sci. 269, 2395-2399.
Pammenter, N.W., Van der Willigen, C., 1998. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol. 18, 589-593.
Passioura, J., 2006. Increasing crop productivity when water is scarce from breeding to field management. Agr. Water Manage. 80, 176-196.
Roddy, A.B., Brodersen, C.R., Dawson, T.E., 2016. Hydraulic conductance and the maintenance of water balance in flowers. Plant Cell Environ. 41, 2123-2132.
Roddy, A.B., Simonin, K.A, McCulloh, K.A., et al., 2018. Water relations of Calycanthus flowers:hydraulic conductance, capacitance, and embolism resistance. Plant Cell Environ. 41, 2250-2262.
Rodriguez-Dominguez, C.M., Carins Murphy, M.R., Lucani, C., et al., 2018. Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytol. 218, 1025-1035.
Schindelin, J., Arganda-Carreras, I., Frise, E., et al., 2012. Fiji:an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
Skelton, R.P., Brodribb, T.J., Choat, B., 2017. Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol. 214, 561-569.
Skelton, R.P., Dawson, T.E., Thompson, S.E., et al., 2018. Low vulnerability to xylem embolism in leaves and stems of North American Oaks. Plant Physiol. 77, 1066-1077.
Sperry, J.S., 2003. Evolution of water transport and xylem structure. Int. J. Plant Sci. 164, S115-S127.
Tyree, M.T., Ewers, F.W., 1991. The hydraulic architecture of trees and other woody plants, New Phytol. 119, 345-360.
Urli, M., Porte, A.J., Cochard, H., et al., 2013. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol. 33, 672-683.
van der Niet, T., Johnson, S.D., 2012. Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol. Evol. 27, 353-361.
Zhang, F.P, Brodribb, T.J., 2017. Are flowers vulnerable to xylem cavitation during drought? Proc. Roy. Soc. B Biol. Sci. 284, 20162642.
Zhang, F.P., Carins Murphy, M.R., Cardoso, A.A., et al., 2018. Similar geometric rules govern the distribution of veins and stomata in petals, sepals and leaves. New Phytol. 219, 1224-1234.
Zimmermann, M.H., 1978. Hydraulic architecture of some diffuse-porous trees. Can. J. Bot. 56, 2286-2295.
Zimmermann, M.H., 1983. Xylem Structure and the Ascent of Sap. Springer Berlin Heidelberg, Berlin/Heidelberg, Germany.

[1]	Yan Ke, Feng-Ping Zhang, Yun-Bing Zhang, Wei Li, Qin Wang, Da Yang, Jiao-Lin Zhang, Kun-Fang Cao. Convergent relationships between flower economics and hydraulic traits across aquatic and terrestrial herbaceous plants[J]. Plant Diversity, 2023, 45(05): 601-610.
[2]	Hong Qian, Shenhua Qian. Geographic patterns of taxonomic and phylogenetic β-diversity of angiosperm genera in regional floras across the world[J]. Plant Diversity, 2023, 45(05): 491-500.
[3]	Jin-Feng Wu, Dong-Rui Jia, Rui-Juan Liu, Zhi-Li Zhou, Lin-Lin Wang, Min-Yu Chen, Li-Hua Meng, Yuan-Wen Duan. Multiple lines of evidence supports the two varieties of Halenia elliptica (Gentianaceae) as two species[J]. Plant Diversity, 2022, 44(03): 290-299.
[4]	Pisal Chheang, David H. Hembry, Gang Yao, Shi-Xiao Luo. Diversity and species-specificity of brood pollination of leafflower trees (Phyllanthaceae: Glochidion) by leafflower moths (Lepidoptera: Epicephala) in tropical Southeast Asia (Cambodia)[J]. Plant Diversity, 2022, 44(02): 191-200.
[5]	Hong Yang, Ping Li, Guihua Jin, Daping Gui, Li Liu, Chengjun Zhang. Temporal regulation of alternative splicing events in rice memory under drought stress[J]. Plant Diversity, 2022, 44(01): 116-125.
[6]	Mi-Cai Zhong, Xiao-Dong Jiang, Wei-Hua Cui, Jin-Yong Hu. Expansion and expression diversity of FAR1/FRS-like genes provides insights into flowering time regulation in roses[J]. Plant Diversity, 2021, 43(02): 173-179.
[7]	Fei-Hong Yan, Li-Ping Zhang, Fang Cheng, Dong-Mei Yu, Jin-Yong Hu. Accession-specific flowering time variation in response to nitrate fluctuation in Arabidopsis thaliana[J]. Plant Diversity, 2021, 43(01): 78-85.
[8]	EiEi Shwe, Bo Wu, Shuang-Quan Huang. Both small and large plants are likely to produce staminate (male) flowers in a hermaphrodite lily[J]. Plant Diversity, 2020, 42(03): 142-147.
[9]	Yonglu Wei, Jianpeng Jin, Xiani Yao, Chuqiao Lu, Genfa Zhu, Fengxi Yang. Transcriptome Analysis Reveals Clues into leaf-like flower mutant in Chinese orchid Cymbidium ensifolium[J]. Plant Diversity, 2020, 42(02): 92-101.
[10]	Ruisen Lu, Wuqin Xu, Qixiang Lu, Pan Li, Jocelyn Losh, Faiza Hina, Enxiang Li, Yingxiong Qiu. Generation and classification of transcriptomes in two Croomia species and molecular evolution of CYC/TB1 genes in Stemonaceae[J]. Plant Diversity, 2018, 40(06): 253-264.
[11]	Yan Zheng, Landi Luo, Yuanyuan Liu, Yunqiang Yang, Chuntao Wang, Xiangxiang Kong, Yongping Yang. Effect of vernalization on tuberization and flowering in the Tibetan turnip is associated with changes in the expression of FLC homologues[J]. Plant Diversity, 2018, 40(02): 50-56.
[12]	Xue Dong, Xiaodong Jiang, Guoqiang Kuang, Qingbo Wang, Micai Zhong, Dongmin Jin, Jinyong Hu. Genetic control of flowering time in woody plants: Roses as an emerging model[J]. Plant Diversity, 2017, 39(02): 104-110.
[13]	Xinhua Li, Licun Zhang, Wenhui Li, Xiaoming Yin, Sen Yuan. New taxa of Berberis (Berberidaceae) with greenish flowers from a biodiversity hotspot in Sichuan Province, China[J]. Plant Diversity, 2017, 39(02): 94-103.
[14]	Ye Chen, Gao Chen, Jing Yang, Weibang Sun. Reproductive biology of Magnolia sinica (Magnoliaecea), a threatened species with extremely small populations in Yunnan, China[J]. Plant Diversity, 2016, 38(05): 253-258.
[15]	Xiong Li1,2,§, Yunqiang Yang1,2,§, Shihai Yang3,§, Xudong Sun1,2, Xin Yin1,2,4, . Comparative proteomics analyses of intraspecific differences in the response of Stipa purpurea to drought[J]. Plant Diversity, 2016, 38(02): 124-145.

Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

Cavitation resistance of peduncle, petiole and stem is correlated with bordered pit dimensions in Magnolia grandiflora

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

本文评价