Water- and carbon-related physiological mechanisms underlying the decline of wild apricot trees in Ili, Xinjiang, China

doi:10.17521/cjpe.2023.0110

Abstract

Abstract:

Aims Wild apricot (Prunus armeniaca var. ansu) in Xinjiang of China, one of the origin species of apricot cultivars around the world, has important economical and ecological values, whereas natural apricot forests in Xinjiang have experienced serious decline and mortality in recent years. It is of great significance to carry out research on the underlying mechanisms for the conservation and recovery of wild apricots in Xinjiang.

Methods In the present study, the xylem hydraulic properties and tissue non-structural carbohydrate (NSC) contents of relatively healthy (dead branches ≤30%) and seriously declined (dead branches ≥70%) wild apricot trees in Ili, Xinjiang were compared to analyze the potential role of hydraulic dysfunction and carbon imbalance in mediating the decline and mortality of this species.

Important findings The results showed that the seriously declined apricot trees had significantly lower leaf area at the branch level, but there were no significant differences in leaf mass per area, relative chlorophyll content and stomatal conductance between the severely declined and relatively healthy trees. The midday leaf water potential, branch hydraulic efficiency and embolism resistance of seriously declined apricot trees were significantly lower than those of relatively healthy ones, indicating an evident xylem hydraulic impairment. The total NSC content of seriously declined trees was lower than that of relatively healthy trees, but the soluble sugar-to-starch content ratio in the stem xylem of seriously declined trees was significantly higher. Impaired hydraulic functioning was accompanied by decreased carbon assimilation capacity and reduced NSC reserve. On top of hydraulic dysfunction, carbon imbalance further contributed to the weakening of tree defense against scale insects, eventually leading to the decline and mortality of apricot trees due to the interplay between plant water relations and carbon economy.

Key words: Prunus armeniaca var. ansu, tree mortality, hydraulic dysfunction, carbon imbalance

OUYANG Yi-Lei, GONG Xue-Wei, DUAN Chun-Yang, ZHANG Chi, MA Chen-Yang, HAN Peng, ZHANG Yuan-Ming, HAO Guang-You. Water- and carbon-related physiological mechanisms underlying the decline of wild apricot trees in Ili, Xinjiang, China[J]. Chin J Plant Ecol, 2024, 48(9): 1192-1201.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2023.0110

https://www.plant-ecology.com/EN/Y2024/V48/I9/1192

Figures/Tables 7

Fig. 1 Relatively healthy (A) and severely declined (B) Prunus armeniaca var. ansu populations in the West Tianshan National Nature Reserve, Xinjiang.

Fig. 2 Differences in sapwood-specific hydraulic conductivity (Ks) (A), maximum sapwood-specific hydraulic conductivity (Ks-max) (B), leaf-specific hydraulic conductivity (Kl) (C) and percentage loss of hydraulic conductivity (PLC) (D) between relatively healthy and severely declined Prunus armeniaca var. ansu trees in the West Tianshan National Nature Reserve, Xinjiang (mean ± SE). Different lowercase letters represent significant differences between the two types of trees (p < 0.05, t-test).

Fig. 3 Percentage loss of hydraulic conductivity (PLC) in response to stem xylem pressure for relatively healthy and severely declined Prunus armeniaca var. ansu trees in the West Tianshan National Nature Reserve, Xinjiang (mean ± SE). P50 and P88 represent xylem pressures leading to 50% and 88% loss of hydraulic conductivity, respectively.

Table 1 Differences in ecophysiological characteristics of Prunus armeniaca var. ansu trees with different states of health in the West Tianshan National Nature Reserve, Xinjiang (mean ± SE)

生理生态参数 Ecophysiological characteristics	相对健康 Relatively healthy	严重衰退 Severely declined
相对叶绿素含量 (SPAD值) Relative chlorophyll content (SPAD value)	41.7 ± 0.95^a	35.55 ± 3.28^a
气孔导度 Stomatal conductance (mmol·m^-2·s^-1)	239.45 ± 15.82^a	210.73 ± 33.06^a
比叶质量 Leaf mass per area (g·m^-2)	65.78 ± 3.61^a	64.06 ± 3.17^a
木材密度 Wood density (g·cm^-3)	0.67 ± 0.02^a	0.58 ± 0.01^b
胡伯尔值 Huber value (×10^-6)	85.86 ± 7.96^b	125.71 ± 12.95^a
凌晨水势 Predawn water potential (MPa)	-0.26 ± 0.04^a	-0.28 ± 0.02^a
正午水势 Midday water potential (MPa)	-1.69 ± 0.22^a	-2.35 ± 0.16^b

Fig. 4 Frequency distribution of stem vessel diameter for relatively healthy and severely declined Prunus armeniaca var. ansu trees in the West Tianshan National Nature Reserve, Xinjiang.

Fig. 5 Differences in the contents of starch, soluble sugar, total non-structural carbohydrate (TNSC) and the soluble sugar-to-starch content ratio in relatively healthy and severely declined Prunus armeniaca var. ansu trees in the West Tianshan National Nature Reserve, Xinjiang (mean ± SE). Different lowercase letters represent significant differences between the two types of trees (p < 0.05, t-test).

Fig. 6 Regression between the soluble sugar and starch contents in xylem of branches of Prunus armeniaca var. ansu trees in the West Tianshan National Nature Reserve, Xinjiang.

References 42

[1]	Abrantes J, Campelo F, García-González I, Nabais C (2013). Environmental control of vessel traits in Quercus ilex under Mediterranean climate: relating xylem anatomy to function. Trees, 27, 655-662.
[2]	Alder NN, Pockman WT, Sperry JS, Nuismer S (1997). Use of centrifugal force in the study of xylem cavitation. Journal of Experimental Botany, 48, 665-674.
[3]	Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012). The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences of the United States of America, 109, 233-237. DOI PMID
[4]	Cai J, Tyree MT (2010). The impact of vessel size on vulnerability curves: data and models for within-species variability in saplings of aspen, Populus tremuloides Michx. Plant, Cell & Environment, 33, 1059-1069.
[5]	Cardoso AA, Batz TA, McAdam SAM (2020). Xylem embolism resistance determines leaf mortality during drought in Persea americana. Plant Physiology, 182, 547-554.
[6]	Chen ZC, Zhu SD, Zhang YT, Luan JW, Li S, Sun PS, Wan XC, Liu SR (2020). Tradeoff between storage capacity and embolism resistance in the xylem of temperate broadleaf tree species. Tree Physiology, 40, 1029-1042. DOI PMID
[7]	Davis SD, Ewers FW, Sperry JS, Portwood KA, Crocker MC, Adams GC (2002). Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure. American Journal of Botany, 89, 820-828.
[8]	Franklin JF, Shugart HH, Harmon ME (1987). Tree death as an ecological process. BioScience, 37, 550-556.
[9]	Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant, Cell & Environment, 40, 831-845.
[10]	Richter H (1997). Water relations of plants in the field: some comments on the measurement of selected parameters. Journal of Experimental Botany, 48, 1-7.
[11]	Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees-from what we can measure to what we want to know. New Phytologist, 211, 386-403. DOI PMID
[12]	Hoch G, Körner C (2003). The carbon charging of pines at the climatic treeline: a global comparison. Oecologia, 135, 10-21. PMID
[13]	Huang JB, Kautz M, Trowbridge AM, Hammerbacher A, Raffa KF, Adams HD, Goodsman DW, Xu CG, Meddens AJH, Kandasamy D, Gershenzon J, Seidl R, Hartmann H (2020) Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling. New Phytologist, 225, 26-36. DOI PMID
[14]	Jacquet JS, Bosc A, O’Grady A, Jactel H (2014). Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiology, 34, 367-376.
[15]	Jansen S, Choat B, Pletsers A (2009). Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. American Journal of Botany, 96, 409-419. DOI PMID
[16]	Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011). Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist, 190, 709-723.
[17]	Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S (2013). Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology, 16, 287-292. DOI PMID
[18]	Li LP, Hai Y, Anwar M, Tang ZY, Fang JY (2011). Community structure and conservation of wild fruit forests in the Ili valley, Xinjiang. Arid Zone Research, 28, 60-66.
	[李利平, 海鹰, 安尼瓦尔·买买提, 唐志尧, 方精云(2011). 新疆伊犁地区野果林的群落特征及保护. 干旱区研究, 28, 60-66.]
[19]	Li M, Hoch G, Körner C (2002). Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees, 16, 331-337.
[20]	Machado RAR, Arce CCM, Ferrieri AP, Baldwin IT, Erb M (2015). Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta. New Phytologist, 207, 91-105.
[21]	McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008). Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist, 178, 719-739. DOI PMID
[22]	McDowell NG (2011). Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology, 155, 1051-1059. DOI PMID
[23]	McDowell NG, Fisher RA, Xu CG, Domec JC, Hölttä T, MacKay DS, Sperry JS, Boutz A, Dickman L, Gehres N, Limousin JM, Macalady A, Martínez-Vilalta J, Mencuccini M, Plaut JA, et al.(2013). Evaluating theories of drought- induced vegetation mortality using a multimodel-experiment framework. New Phytologist, 200, 304-321. DOI PMID
[24]	Mediene S, Jordan MO, Pagès L, Lebot J, Adamowicz S (2002). The influence of severe shoot pruning on growth, carbon and nitrogen status in young peach trees (Prunus persica). Tree Physiology, 22, 1289-1296. PMID
[25]	O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014). Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nature Climate Change, 4, 710-714.
[26]	Roth M, Hussain A, Cale JA, Erbilgin N (2018). Successful colonization of lodgepole pine trees by mountain pine beetle increased monoterpene production and exhausted carbohydrate reserves. Journal of Chemical Ecology, 44, 209-214. DOI PMID
[27]	Šimpraga M, Takabayashi J, Holopainen JK (2016). Language of plants: Where is the word. Journal of Integrative Plant Biology, 58, 343-349.
[28]	Singh V, Mandhania S, Pal A, Kaur T, Banakar P, Sankaranarayanan K, Arya SS, Malik K, Datten R (2022). Morpho-physiological and biochemical responses of cotton (Gossypium hirsutum L.) genotypes upon sucking insect-pest infestations. Physiology and Molecular Biology of Plants, 28, 2023-2039.
[29]	Sobrado MA (2003). Hydraulic characteristics and leaf water use efficiency in trees from tropical montane habitats. Trees, 17, 400-406.
[30]	Sperry JS, Wang YJ, Wolfe BT, Mackay DS, Anderegg WRL, McDowell NG, Pockman WT (2016). Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. New Phytologist, 212, 577-589. DOI PMID
[31]	Tomasella M, Häberle KH, Nardini A, Hesse B, Machlet A, Matyssek R (2017). Post-drought hydraulic recovery is accompanied by non-structural carbohydrate depletion in the stem wood of Norway spruce saplings. Scientific Reports. 7, 14308. DOI: 10.1038/s41598-017-14645-w.
[32]	Tomasella M, Nardini A, Hesse BD, Machlet A, Matyssek R, Häberle KH (2019). Close to the edge: effects of repeated severe drought on stem hydraulics and non-structural carbohydrates in European beech saplings. Tree Physiology, 39, 717-728. DOI PMID
[33]	Tyree MT, Sperry JS (1989). Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 19-36.
[34]	Vandegehuchte MW, Bloemen J, Vergeynst LL, Steppe K (2015). Woody tissue photosynthesis in trees: salve on the wounds of drought. New Phytologist, 208, 998-1002. DOI PMID
[35]	Venturas MD, Sperry JS, Hacke UG (2017). Plant xylem hydraulics: What we understand, current research, and future challenges. Journal of Integrative Plant Biology, 59, 356-389. DOI
[36]	Wang YL, Lyu ZZ, Linghu W, Gao GZ (2021). Sphaerolecanium prunastri (Hemiptera: Coccoidea: Coccidae), a new pest in wild fruit forests, Xinjiang. Forest Research, 34, 152-158.
	[王玉丽, 吕昭智, 令狐伟, 高桂珍 (2021). 新疆野果林的新害虫——杏树鬃球蚧(半翅目: 蚧总科: 蚧科). 林业科学研究, 34, 152-158.]
[37]	Wang YL, Lyu ZZ, Linghu W, Wang Q, Gao GZ (2022). Occurrence and harm of Sphaerolecanium prunastri in wild fruit forests in Xinjiang. Xinjiang Agricultural Sciences, 59, 1741-1747.
	[王玉丽, 吕昭智, 令狐伟, 王强, 高桂珍 (2022). 新疆野果林杏树鬃球蚧的发生及危害. 新疆农业科学, 59, 1741-1747.] DOI
[38]	Wiley E, Rogers BJ, Hodgkinson R, Landhäusser SM (2016). Nonstructural carbohydrate dynamics of lodgepole pine dying from mountain pine beetle attack. New Phytologist, 209, 550-562. DOI PMID
[39]	Yang QX, Liu LQ, Qin W, Diao YQ, Zhao ZJ, Wu RQMG, Zhang B (2022). Population structure characteristics and health evaluation of Prunus armeniaca Lam. Chinese Journal of Ecology, 41, 9-17.
	[杨其享, 刘立强, 秦伟, 刁永强, 赵忠晶, 乌仁其米格, 张博 (2022). 新疆野杏种群结构特征与健康评价. 生态学杂志, 41, 9-17.]
[40]	Zhang JL, Cao KF (2009). Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Functional Ecology, 23, 658-667.
[41]	Zhang YM, He TM, Feng JR, Chen MX, Yuan ZH, Sun JZ, Zhang DH, Wu Y, Zhang LJ, Chen XS (2009). New advances of the apricot resources evaluation, germplasm enhancement and utilization. Acta Horticulturae Sinica, 36, 755-762.
	[张艳敏, 何天明, 冯建荣, 陈美霞, 苑兆和, 孙家正, 张大海, 吴燕, 张立杰, 陈学森 (2009). 杏种质资源评价、创新与利用研究新进展. 园艺学报, 36, 755-762.]
[42]	Zhao F, Liu WS, Liu N, Yu XH, Sun M, Zhang YP, Zhou YQ (2005). Reviews of the apricot germplasm resources and genetic breeding in China. Journal of Fruit Science, 22, 687-690.
	[赵锋, 刘威生, 刘宁, 郁香荷, 孙猛, 张玉萍, 周晏起 (2005). 我国杏种质资源及遗传育种研究新进展. 果树学报, 22, 687-690.]