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/lp/springer-journals/differences-in-eco-physiological-responses-to-the-removal-of-zwHyOD7CY0
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- Springer Journals
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- Copyright © The Author(s) 2023
- ISSN
- 1286-4560
- eISSN
- 1297-966X
- DOI
- 10.1186/s13595-023-01180-0
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Abstract
Key message The production of adventitious roots partially counteracts the negative effects of waterlogging on the growth of Syzygium nervosum A. Cunn. ex DC. and Syzygium cumini (L.) Skeels. S. cumini was more responsive and suf- fered from larger negative effects than S. nervosum after the removal of adventitious roots. Context Adventitious roots contain gas channels and functionally replace or compensate for the loss of primary roots that usually decay during waterlogging. However, the importance of adventitious roots on growth in water- logged woody plants varies with species. Therefore, there has been some controversy about whether adventitious roots have beneficial effects on the growth of waterlogged plants. Aims We assessed whether S. nervosum and S. cumini differentially responded to the ablation of adventitious roots during waterlogging and whether compensatory responses occurred in the primary roots in both species. Methods S. nervosum and S. cumini saplings were subjected to waterlogging and adventitious root removal for 120 days, and morphological, physiological, biochemical parameters, and biomass were recorded. Results All plants survived waterlogging, and produced adventitious roots at the shoot base. Waterlogging had negative effects on the growth of both species, but the effect was more severe in S. cumini than in S. nervosum as seen from the values of comprehensive evaluation and total biomass. However, S. nervosum compensated for the ablation of adventitious roots with increased primary root dry mass, primary root activity, total root length, root tip number, and peroxidase activity. Conclusions S. nervosum with a high proportion of adventitious roots would be at an advantage during waterlog- ging. The removal of adventitious roots was detrimental to the growth of both species, but S. nervosum exhibited less damage than S. cumini due to its compensatory physiological responses and its primary roots. Handling editor: Erwin Dreyer. *Correspondence: Fan Yang fanyangmlf6303@163.com; yangfan@hainanu.edu.cn Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Li et al. Annals of Forest Science (2023) 80:13 Page 2 of 14 Keywords Adventitious roots removal, Compensatory response, Root system development, Waterlogging potential, and photosynthetic capacity of waterlogged 1 Introduction crops and herbaceous plants (Muhammad 2012). According to the Intergovernmental Panel on Climate The removal of adventitious roots had negative effects Change, the global average temperature is predicted on photosynthesis, leaf initiation and expansion, growth to increase by 1.4 °C to 5.8 °C over the period from rates, and dry weight in some crops and herbaceous 1990 to 2100 (IPCC 2013), which will lead to increased plants like Alternanthera philoxeroides (Mart.) Griseb., intensity and frequency of extreme precipitation events Cotula coronopifolia L., Meionectes brownii Hook. f. (syn. at the global scale (Tabari et al. 2019). Therefore, under - Haloragis brownii), Platanus occidentalis L., and Sola- standing how plant growth responds to a future wet- num dulcamara L. (Tsukahara and Kozlowski 1986; Rich ter environment is crucial, particularly in tropical and et al. 2012; Ayi et al. 2016; Zhang et al. 2017). However, subtropical regions. Waterlogging negatively affects the in contrast to these results, relatively few documents diffusion of O into the soil and reduces the O con- 2 2 reported that the removal of adventitious roots did not tent in waterlogged soils (Drew 1983), thus inhibiting adversely affect Epilobium hirsutum L. and Alnus glu- root respiration and resulting in decreased levels of tinosa (L.) Gaertn. and even increased the biomass and plant growth and photosynthesis rates, and even death total shoot height of Lythrum salicaria L. (Gill 1975; (Kozlowski 1986, 1997). Stevens and Peterson 2007). Therefore, there has been Plants have evolved morphological, physiological, some controversy about whether adventitious roots have and biochemical responses to cope with waterlogging- beneficial effects on the growth of waterlogged plants or induced hypoxia (Insausti et al. 2001; Vashisht et al. whether they are merely non-functional expressions of 2011; Zhang et al. 2015). Changes in the biomass allo- waterlogging injury. Since the waterlogging tolerance and cation can be an important mechanism to improve the occurrence of injuries is strongly species-dependent, plant performance under environmental stress (Baz- and knowledge on physiological and molecular aspects of zaz et al. 1987). However, controversial results on waterlogging tolerance in woody plants is far behind that the effects of waterlogging on biomass allocation are of herbaceous species (Kreuzwieser et al. 2009; Kreu- still observed. For example, some studies have dem- zwieser and Rennenberg 2014). Thus, quantifying the onstrated that waterlogging led to either higher or importance of adventitious roots on the growth of water- lower allocation to roots in plants (Lenssen et al. 2003; logged woody plants is essential. Ye et al. 2003), while Wu et al. (2018) reported that S. nervosum (also named as Cleistocalyx operculatus) waterlogging had no effect on the root/shoot ratio in and S. cumini are two waterlog-tolerant trees of South Triticum aestivum. Waterlogging causes a remarkable China, which play a very important role in the restora- increase in the storage of non-structural carbohydrates tion of riparian zones (Jing et al. 2001; Ma et al. 2019; in many species (Limpinuntana and Greenway 1979; Yang et al. 2022). S. nervosum and S. cumini actually pro- Daugherty and Musgrave 1994). This storage serves as duced adventitious roots during waterlogging, and S. ner- a carbon buffer, allowing plant survival in hypoxic con - vosum has higher adventitious root production than S. ditions when aerobic ATP production cannot meet the cumini (Li et al. 2022a). We hypothesized that larger neg- demands of a plant (Voesenek and Bailey-Serres 2015). ative effects of adventitious root removal happen in the Meanwhile, waterlogging can also lead to rapid accu- S. nervosum saplings with more adventitious roots than mulation or degradation of plant hormones and regu- in S. cumini saplings. We further explored whether com- lates the response of plants to waterlogging via complex pensatory responses in the primary roots would occur in signaling (Pan et al. 2021). In addition, plants possess both species. To test our hypothesis, we quantified the a suite of antioxidant enzyme systems and produce changes in morphologic traits, biomass accumulation, some osmoregulatory substances, like free proline, to and related physiological and biochemical parameters of alleviate membrane lipid peroxidation caused by the S. nervosum and S. cumini saplings caused by the removal accumulation of reactive oxygen species (ROS) under of adventitious roots. waterlogging (Yang et al. 2011). On the other hand, plant responses to waterlogging frequently involve the production of adventitious roots, which could func- 2 Materials tionally replace or compensate for the loss of primary 2.1 Plant material and experimental design roots that usually decay during waterlogging. In turn Two-year-old saplings of S. nervosum and S. cumini this can improve the hydraulic conductivity, leaf water were obtained as previously described (Li et al. 2022a). Li et al. Annals of Forest Science (2023) 80:13 Page 3 of 14 To ensure uniform growth after retillering, each sap- dry mass (the sum of primary roots and adventitious root ling was cut at 5 cm above the soil surface. All saplings dry mass) and the aboveground dry mass (the sum of leaf without attached soil balls were transplanted into 5-l and stem dry mass). plastic pots containing sand and red soil (2:1, v/v) and were grown (one sapling planted in each pot) in a green- 2.3 Determination of net photosynthetic rate house at Hainan University (20°3′ N, 110°19′ E), which and chlorophyll content only blocked ambient rainfall but otherwise maintained The fourth fully expanded and exposed leaves were ambient light and temperature. All saplings were watered selected from the apex of each sapling to determine the regularly and allowed to maintain the soil water con- net photosynthetic rate and stomatal conductance by tent close to field capacity. The sandy soil contained 5.34 using a portable photosynthesis system (TP-3051D, Zhe- −1 −1 mg kg ammoniacal nitrogen, 11.78 mg kg available jiang, China): temperature, 30 °C; light intensity, 1400 −1 -2 -1 phosphorus, and 81.72 mg kg available potassium. The μmol photons·m ·s ; relative humidity, 60%; and ambi- -1 annual mean rainfall, temperature, and insulation time in ent CO , 350 ± 5 μmol mol . The net photosynthetic rate this area are 1715.3 mm, 24.4 °C, and 2000 h, respectively and stomatal conductance were measured from 8:30 to (Li et al. 2022a). After 3 months, saplings with similar 11:30 a.m. on 29 and 30 September 2019. The content of growing status were selected for the experiments. chlorophyll pigments was measured in the same leaves. A 2 × 3 factorial design included two species (i.e., Leaf samples (~0.2 g of fresh sample) were extracted in S. nervosum and S. cumini) and three treatments (i.e., 10 mL of 80% chilled acetone. After centrifugation at control; waterlogging; adventitious root removal dur- 3000 rpm and 4 °C for 3 min, the supernatant was used ing waterlogging). Controls were watered regularly with for the determination of chlorophyll content. The absorb - tap water to maintain the soil water content close to field ance of supernatant was recorded at 663 nm, 645 nm, and capacity. For the waterlogging treatment, the saplings 470 nm, respectively. Chlorophyll a, chlorophyll b, and were partially submerged in a big plastic bucket filled carotenoid concentration were calculated as described by with tap water (flooded 15 cm above soil surface). For the Lichtenthaler (1987). The sum of chlorophyll a and chlo - adventitious root removal treatment, adventitious roots rophyll b was defined as the total chlorophyll. were removed using a razor blade under the water sur- face as soon as the primordial of the adventitious roots 2.4 Determination of peroxidase, free proline, was visible (∼5 mm in length). The solution was entirely and malondialdehyde (MDA) replaced every 14 days. Twenty-five saplings were used The peroxidase activity was measured spectrophotomet - per treatment (five replicates, and five saplings per repli - rically at 470 nm as previously described (Li et al. 2022a), cate). The treatment lasted for 120 days (from June 2019 using guaiacol as substrate. One unit of peroxidase activ- to October 2019). ity was defined as the amount of enzyme that caused an increase of 0.01 in the absorbance per minute under −1 2.2 A nalyses of plant morphology and biomass standard conditions. The content of free proline (μg·g The shoot length of each sapling was measured at the FW) was measured using the acid ninhydrin method end of the growing season. Then, all saplings were sam - given by Bates et al. (1973). The absorbance was recorded −1 pled and divided into leaves, shoots, primary roots, and at 520 nm. Malondialdehyde (μmol·g FW) content was adventitious roots after washing out the soil (Li et al. determined using the 2-thiobarbituric acid method as 2023). The total leaf area per sapling was measured using described by Li et al. (2022a). a leaf area meter (LI-3000C, Li-Cor, Inc., Lincoln, NE, USA). The primary roots of each sapling were scanned 2.5 Determination of leaf midday water potential, relative with a double-lamp bed scanner (Epson 12000XL, Los water content, and primary root activity Alamitos, CA, USA) at 400 dpi. The total root length On 29 and 30 September 2019, the 12:00 to 14:00 leaf water and number of root tips number were analyzed with potential of each sapling was recorded using a WP4C Dew- Win-RHIZO (Regent Instruments, Inc., Neplean, ON, point hygrometer (Decagon Devices, Inc., Pullman, WA, Canada). Finally, all tissues were oven-dried at 70 °C to USA) according to the method of Liao et al. (2019). After a constant mass, and weighed. Whole-plant relative the measurement of leaf water potential, the leaf samples growth rate (RGR ) was calculated as RGR = (b – b )/t, were collected to record the relative water content. Samples t 0 where b represents the initial, b is the final total biomass were dried in a forced-air oven at 70 °C till a constant dry 0 t of each sapling, and t is the treatment time in days. Lea- weight was obtained. The primary root activity was meas - farea ratio was calculated as the ratio of total leaf area to ured by the triphenyl tetrazolium chloride method accord- total plant dry weight. The belowground/aboveground ing to Ruf and Brunner (2003). In detail, fresh primary root ratio was calculated as the ratio between the total root samples (∼0.2 g) from each sapling were selected, cut into Li et al. Annals of Forest Science (2023) 80:13 Page 4 of 14 1-cm pieces, and transferred to 10-mL centrifuge tubes anthrone colorimetric method at 620 nm by spectropho- containing 2.5 mL of 1 % triphenyl tetrazolium chloride tometry (Wang et al. 2020). The residues from the extrac - solution and 2.5 mL 0.1 M potassium phosphate buffer (pH tion of the total soluble sugars were transferred to a 25-mL 7.5). The samples were incubated for 1 h at 37 °C in the dark test tube and incubated in 20 mL distilled water at 100 °C −1 and then mixed with 1 mL of l M H SO . The root pieces for 15 min. After incubation, 2 mL 9.2 mol L ice-cooled 2 4 were washed twice with 2 mL of distilled water, and their perchloric acid was added. Then, the samples were incu - surfaces were dried carefully with absorbent papers. Then, bated for 15 min at room temperature, centrifuged at 4000 3 mL of ethyl acetate was added, and the samples were rpm and 4 °C for 10 min. The residues were dissolved in vortexed for 30 s. The samples were centrifuged at 12,000 distilled water (10 mL) and incubated for 15 min at 100 °C. −1 rpm and 4 °C for 3 min. The precipitate was discarded, and The solutions were extracted with 2 mL 4.6 mol L per- ethyl acetate was added to adjust the final volume to 5 mL. chloric acid for 15 min and then centrifuged. Absorbance was measured at 485 nm. The reactivity of the The supernatant was collected, and the residues were samples with triphenyl tetrazolium chloride was expressed washed three times with distilled water. The superna - as absorption of triphenyl tetrazolium formazan per milli- tant and the washing water were combined, and distilled −1 −1 gram fresh weight (mg·g ·h ·FW). water was added to adjust the final volume to 100 mL. The absorbance was measured at 620 nm. The sum of sugars and starch were presented as non-structural carbohydrate. 2.6 Det ermination of non‑structural carbohydrate of leaves The dried and fine-ground leaf sample (∼ 0.05 g) from each 2.7 Determination of phytohormone contents sapling were transferred to 10-mL centrifuge tubes, incu- After the net photosynthetic rate measurements, the bated in 80% ethanol at 80 °C for 30 min and centrifuged at uppermost fully expanded fresh leaf samples (∼0.5 g) 12,000 rpm and 4 °C for 5 min. The ethanolic extracts were from each sapling were carefully collected from 8:30 a.m. used to determine the total soluble sugars by using the to 10:30 a.m. The samples were immediately frozen in Fig. 1 Aboveground (a) and belowground (b) growth response of S. nervosum and S. cumini saplings to waterlogging with or without adventitious root removal. Treatment: CK, well-watered; WL, waterlogging; AR-R, adventitious root removal Li et al. Annals of Forest Science (2023) 80:13 Page 5 of 14 liquid nitrogen and extracted in cold 80% (v/v) metha- significant at the p < 0.05 level. Additionally, we used a nol with butylated hydroxytoluene (1 mmol/L) over- comprehensive evaluation method to evaluate the growth night at 4°C, centrifuged at 10,000 rpm and 4 °C for 20 status. Given the large dataset, the principal compo- min. The supernatant was passed through a C Sep-Pak nent analysis was carried out on all the variables (except cartridge (Waters, Milford, MA, USA) and dried in N . adventitious root mass) of both species for dimension The levels of auxin (IAA), abscisic acid (ABA), gibberel - reduction, and we obtained two eigenvalues (the first two lic acid (GA ) and zeatin riboside (ZR) were determined components comprised about 85% of the total variance). by enzyme-linked immune sorbent assay (ELISA) accord- Membership function value of each selected eigenvalue ing to the method of Yang et al. (2001). All measurements was calculated (Yan et al. 2022), and final comprehen - were performed in the Key Laboratory of Molecular sive evaluation value was obtained using the membership Plant Pathology, Ministry of Agriculture, Beijing, China. function value (Xiang et al. 2021). The maximum value was considered as the optimal growth status. 2.8 Statistical analysis All statistical analyses were performed using the SPSS 13.0 3 Results (IBM Inc., Chicago, IL, USA). Data for each of the meas-3.1 Growth traits ured traits were tested for normality and homoscedastic- All saplings survived after 120 days of waterlogging ity before analysis. Data without normal distribution were treatment, but their growth was considerably inhib- transformed logarithmically. Duncan’s multiple range test ited, especially in S. cumini (Fig. 1). Adventitious root was used to analyze the differences among treatments. An removal induced the formation of floating roots from independent-sample t test was conducted to determine the primary roots in S. nervosum, but not in S. cumini differences between the two species. Two-factor analy - (Fig. 2). In addition, the waterlogging resulted in a sis of variance (ANOVA) with LSD post-hoc tests were decrease of shoot length, total root length, root tip num- used to further determine the effects of waterlogging and ber, whole-plant relative growth rate, and belowground/ adventitious root removal. Differences were considered aboveground biomass (not in S. nervosum) of both Fig. 2 Compensatory growth in S. nervosum after removing the adventitious root. Note: S. nervosum responds to adventitious root removal by growing a large number of floating roots with aerenchyma from the primary roots. Cortex cell layers and lysigenous aerenchyma are indicated by red dashed lines and red arrowheads, respectively Li et al. Annals of Forest Science (2023) 80:13 Page 6 of 14 Fig. 3 Shoot length (a), leaf area ratio (b), total root length (c), root tip number (d), and whole-plant relative growth rate (e) in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious root removal. Treatment: CK, well-watered; WL, waterlogging; AR-R, adventitious root removal. F , waterlogging effect; F , adventitious root removal effect. Data presented are means ± SE (n = 5). Bars with the W AR-R different letter within the same species group indicate significant differences at p<0.05 by analysis of variance (ANOVA). Asterisks above bars denote statistically significant differences between the species according to independent-samples t test. ns, p>0.05; ∗p<0.05; ∗∗p<0.01; ∗∗∗p≤0.001 species (Fig. 3 and Table 1), and significantly increased waterlogging. In addition, compared with the water- the leaf area ratio in S. cumini (Fig. 3b). Adventitious logging treatment, adventitious root removal treat- root removal also resulted in similar trends as it did in ment resulted in decreased belowground/aboveground Li et al. Annals of Forest Science (2023) 80:13 Page 7 of 14 Table 1 Biomass accumulation and allocation in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious root removal Species Treatment ARM PRM SM LM TM BA ‑1 ‑1 ‑1 ‑1 ‑1 (g • plant DM) (g • plant DM) (g • plant DM) (g • plant DM) (g • plant DM) S. nervosum CK n.a. 5.62±0.17 Ans 7.98±0.54 A*** 3.11±0.05 A*** 16.7±0.57 A*** 0.51±0.03 A*** WL 1.93±0.17*** 1.56±0.08 C*** 4.66±0.28 B*** 2.81±0.2 AB*** 10.96±0.31 B*** 0.47±0.02 A*** AR-R n.a. 1.98±0.11 B*** 4.21±0.37 B*** 2.63±0.09 Bns 8.83±0.32 C** 0.29±0.02 B*** F n.a. 0.000*** 0.000*** 0.134 ns 0.000*** 0.186 ns F n.a. 0.039* 0.457ns 0.349 ns 0.003** 0.000*** AR-R S. cumini CK n.a. 4.94±0.35 a 21.76±0.57 a 11.09±0.43 a 37.79±0.84 a 0.15±0.01 a WL 0.70±0.13 0.39±0.04 b 10.86±0.7 b 4.67±0.32 b 16.63±0.65 b 0.07±0.01 b AR-R n.a. 0.34±0.04 b 7.44±0.42 c 3.15±0.21 c 10.94±0.38 c 0.03±0.00 c F n.a. 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** F n.a. 0.862 ns 0.001*** 0.007** 0.000*** 0.011* AR-R Treatment: CK well-watered, WL waterlogging, AR-R adventitious root removal Abbreviations: ARM adventitious root mass, PRM primary root mass, SM stem mass, LM leaf mass, TM total mass, BA the belowground/aboveground ratio. F , waterlogging effect; F , adventitious root removal effect. Data presented are means ± SE (n = 5). Different letters indicate significant differences at p<0.05 by AR-R analysis of variance (ANOVA). Asterisks following capital letters denote statistically significant differences between the species according to independent-samples t test. ns, p>0.05; ∗p<0.05; ∗∗p<0.01; ∗∗∗p≤0.001; n.a., no adventitious roots biomass and whole-plant relative growth rate in both both species. However, the carotenoid/total chlorophyll species, but increased the total root length and root tip and POD activities in S. nervosum and the MDA contents number in the primary roots of S. nervosum by 36.7% in both species were increased. Under adventitious root and 48.1%, respectively. By contrast, adventitious root removal, both species presented the smallest net photo- removal had no effect in S . cumini (Fig. 3c and d). Simi- synthesis rate and stomatal conductance but the high- larly, adventitious root removal treatment significantly est POD, MDA, and free proline. In addition, compared decreased shoot length (decreased by 81.3%) and signifi - with waterlogging, adventitious root removal resulted in cantly increased leaf area ratio (increased by 15.8%) in an increase in the POD in S. nervosum and MDA in S. S. cumini, whereas its effects on S . nervosum were non- cumini. By contrast, net photosynthesis rate in S. cumini significant (Fig. 3 a and b). and stomatal conductance in S. nervosum were signifi - cantly decreased. 3.2 Biomass allocation As shown in Table 1, waterlogging and adventitious root 3.4 Midday leaf water potential, relative water content, removal treatments significantly decreased the dry mass and primary root activity of primary roots, stem, leaf, total plant, and the relative The highest values of midday leaf water potential, rela - growth rate in both species. A larger decrease of these tive water content, and primary root activity were parameters was found in S. cumini than in S. nervosum. S. detected in controls (Fig. 4). Waterlogging and adven- nervosum saplings had a significantly higher dry mass of titious root removal decreased the values of midday adventitious roots than S. cumini. Compared with water- leaf water potential and relative water content and logging, adventitious root removal resulted in decreased the primary root activity in both species with respect dry mass of stem and leaf in S. cumini and total plant dry to controls. Adventitious root removal also resulted mass, and relative growth rate in both species but sig- in decreased midday leaf water potential and relative nificantly increased the dry mass of primary roots in S. water content in S. cumini but significantly increased nervosum. primary root activity in S. nervosum compared to waterlogging. 3.3 G as exchange, peroxidase (POD) activities, chlorophyll, MDA, and free‑proline contents As shown in Table 2, compared to controls, waterlog- 3.5 Non‑structural carbohydrates and phytohormone ging significantly decreased the chlorophyll a and carot - concentrations enoid contents in S. cumini and the net photosynthesis Waterlogging significantly increased total soluble sugar, rate, stomatal conductance, and chlorophyll b contents in starch, and non-structural carbohydrate in both species Li et al. Annals of Forest Science (2023) 80:13 Page 8 of 14 Table 2 Net photosynthesis rate (Pn), stomatal conductance (g ), pigments, peroxidase (POD), malondialdehyde (MDA), and free proline (Pro) of leaves in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious roots removal Species Treatment Pn g Chl a Chl b Caro Caro/Chl POD MDA Pro 2 1 −2 −1 −1 −1 −1 –1 –1 1 −1 (μmol·m ·s ) (mol·m ·s ) (μg·g FW) (μg·g FW) (μg·g FW) (U·min ·g FW) (μmol·g FW) (μg·g FW) S. nervosum CK 8.25±0.99 A** 0.17±0.03 Ans 136.83±11.69 A** 67.65±2.78 Ans 250.44±18.20 A*** 1.25±0.13 B** 32.55±3.00 C** 29.01±0.74 B*** 14.19±1.15 b WL 4.18±0.34 Bns 0.08±0.00 Bns 112.52±3.92 ABns 52.34±1.15 Bns 303.26±18.34 A*** 1.84±0.11 A*** 53.02±0.74 Bns 38.42±1.31 A*** 16.81±0.94 ab AR-R 2.91±0.47 Bns 0.03±0.00 C* 108.14±8.56 Bns 53.48±1.59 Bns 282.35±19.77 A*** 1.75±0.09 A*** 66.36±6.36 Ans 40.68±0.95 A** 17.84±0.64 a F 0.001*** 0.001*** 0.071ns 0.000*** 0.070ns 0.003** 0.004** 0.000*** 0.070ns F 0.442ns 0.035* 0.727ns 0.690ns 0.446ns 0.585ns 0.039* 0.145ns 0.448ns AR-R S. cumini CK 14.24±0.29 a 0.10±0.01 a 206.92±3.45 a 64.64±1.48 a 49.58±3.34 a 0.18±0.01 a 53.78±1.99 a 11.51±0.66 c 30.89±3.48 B** WL 5.14±0.36 b 0.06±0.01 b 126.96±7.00 b 52.22±0.78 b 36.82±3.00 b 0.20±0.01 a 63.45±5.77 a 22.59±1.03 b 44.78±6.50 AB** AR-R 3.66±0.51 c 0.05±0.01 b 137.31±11.44 b 53.25±1.61 b 40.44±1.81 b 0.22±0.02 a 68.65±5.68 a 30.34±2.76 a 48.39±4.89 A** F 0.000*** 0.006** 0.000*** 0.000*** 0.007** 0.350ns 0.181ns 0.001*** 0.079ns F 0.022* 0.237ns 0.378ns 0.597ns 0.378ns 0.568ns 0.460ns 0.008** 0.627ns AR-R Abbreviations: Chl a chlorophyll a, Chl b chlorophyll b, Caro carotenoid, Caro/Chl ratios of carotenoid to total chlorophyll. For abbreviations explanation of treatments and data description and statistics are the same as shown in Table 1 Li et al. Annals of Forest Science (2023) 80:13 Page 9 of 14 Fig. 4 Midday leaf water potential (a), relative leaf water content (b), and primary root activity (d) in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious root removal. The abbreviations, explanation of treatments, and data description and statistics are the same as shown in Fig.3 and GA , ZR, IAA, and ABA contents in S. cumini but sig-4 Discussion nificantly decreased the GA , IAA, and ABA contents in S. 4.1 S. nervosum exhibits superior adaptation nervosum (Figs. 5 and 6). Moreover, compared to waterlog- to waterlogging than S. cumini ging, adventitious root removal resulted in an increase in Relative growth rate and comprehensive evaluation the total soluble sugar (slightly increased in S. nervosum), values are important indicators in identifying water- starch, and non-structural carbohydrate in both species logging tolerance in plants (Gibberd et al. 2001; Ye and the ZR, IAA, and ABA contents in S. cumini but signif- et al. 2003; Zhao et al. 2022). This study clearly dem - icantly decreased the GA , IAA, and ABA in S. nervosum. onstrated that S. nervosum was more tolerant to water- logging than S. cumini. Javier (1987) stated that root 3.6 C omparative comprehensive evaluation aeration is critical in waterlogged soil, thus any plant among different treatments species with a high proportion of adventitious roots As shown in Table 3, two groups of eigenvalues were would be at an advantage. Consequently, S. nervosum obtained after dimensional reduction. The final compre - with a larger adventitious root system can maintain a hensive evaluation values of S. nervosum and S. cumini higher rate of minerals uptake and water and O trans- saplings were sequentially reduced in the controls, water- portation to meet the specific resource demands asso - logging, and adventitious root removal treatments. In ciated with waterlogging (Gill 1975; Rich et al. 2012). other words, both species from the controls possessed This observation is strengthened by the larger decline the best growth status. In addition, S. nervosum always in chlorophyll a content observed in S. cumini. Mean- had higher comprehensive evaluation values than did S. while, the greater relative waterlogging tolerance of cumini in all treatments. S. nervosum appears to also depend on the degree of Li et al. Annals of Forest Science (2023) 80:13 Page 10 of 14 Fig. 5 Total soluble sugar (a), starch (b), and non-structural carbohydrates (c) contents of leaves in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious root removal. The abbreviations, explanation of treatments, and data description and statistics are the same as shown in Fig.3 development of aerenchyma (Malik et al. 2011; Khan waterlogging stress might be closely related to its better et al. 2014). After waterlogging treatment, S. nervosum self-protective ability. Under waterlogging conditions, showed less reduction in belowground/aboveground the accumulation of reactive oxygen species (ROS) can ratio than S. cumini, leading to larger total root length induce lipid peroxidation, chlorophyll degradation, and and root tip number in S. nervosum. According to the loss of photosynthetic activity, while the higher peroxi- viewpoints of Das and Jat (1977), root length increased dase activity ßand carotenoids can efficiently eliminate with root porosity. Thus, higher total root length repre - the massive amount of H O and protecting photosyn- 2 2 sented a larger aerenchyma area, thereby increasing the thetic apparatus from ROS (Li et al. 2012; Liao et al. rate of O diffusion from the shoot to the root, which 2019). On the other hand, the phenomenon may also is essential for the maintenance of aerobic respiration be attributed to the facts that S. nervosum suffered less (Yin et al. 2010). This is consistent with our previous decrease in midday leaf water potential and relative leaf work reporting that Cleistocalyx operculatus (basio- water content and greater reduction in stomatal con- nym of S. nervosum (DC.) Kosterm.) could maintain a ductance. This strategy generally allows for adequate higher porosity of primary roots than S. cumini when gas exchange while minimizing water loss (Gazal and exposed to waterlogging stress (Li et al. 2022a). Addi- Kubiske 2004). Therefore, S . nervosum exhibits superior tionally, the fact that S. nervosum can better withstand adaptation to waterlogging than S. cumini. Li et al. Annals of Forest Science (2023) 80:13 Page 11 of 14 Fig. 6 Gibberellic acid (a), zeatin riboside (b), auxin (c), and abscisic acid (d) contents of leaves in S. nervosum and S. cumini saplings, as affected by waterlogging with or without adventitious root removal. The abbreviations, explanation of treatments, and data description and statistics are the same as shown in Fig. 3 Table 3 Eigenvalue, membership function value, and comprehensive evaluation value in S. nervosum and S. cumini saplings under different treatments Species Treatment C (1) C (2) M (1) M (2) CE S. nervosum CK 0.667 1.450 0.584 1.000 0.750 WL -0.587 0.646 0.086 0.666 0.318 AR-R -0.805 0.474 0.000 0.595 0.238 S. cumini CK 1.718 -0.672 1.000 0.120 0.648 WL -0.254 -0.937 0.218 0.010 0.135 AR-R -0.738 -0.961 0.027 0.000 0.016 C(μ), eigenvalue; M(μ), membership function value; CE comprehensive evaluation value. For abbreviations explanation of treatments are the same as shown in Table 1 4.2 S. nervosum had a compensatory response nervosum has other mechanisms aside from production to adventitious root removal, contrary to S. cumini of adventitious roots which enable the species to survive Adventitious root removal was detrimental to the growth under hypoxic conditions and tolerate waterlogging. The of both species. However, growth reduction was more compensatory growth in primary roots of S. nervosum severe in S. cumini than in S. nervosum as the water- could be a reasonable explanation. This confirms the logging duration was extended. This suggests that S . results obtained by Matsuura et al. (2016) that Panicum Li et al. Annals of Forest Science (2023) 80:13 Page 12 of 14 Code availability sumatrense L. exhibits waterlogging tolerance by enhanc- Not applicable. ing root growth. Meanwhile, this is probably due to the ability of S. nervosum to develop a large number of floating Authors’ contributions F Y designed the study, provided funding and revised the manuscript; DD L roots with aerenchyma as a response to waterlogging of performed the experiments, data collection, and drafted the manuscript; LF M the soil, while S. cumini did not show significant develop - performed data processing and statistics; MJ T, JJ Z and WZ Y performed part ment of floating roots. This notion is strengthened by the of the experiment. All authors read and approved the final manuscript. significant decline in soluble sugar (no change), GA , and Funding ABA content observed in S. nervosum. Because the sugar, This work was supported by the National Natural Science Foundation of China GA , and ABA derived from leaves were essential for (no. 32060240 and 31660165), the Hainan Provincial Natural Science Founda- tion of China (421RC1033), and Hainan Province Science and Technology aerenchyma or adventitious root formation under water- Special Fund (ZDYF2022SHFZ054). logged soil conditions (Takahashi et al. 2018; Cisse et al. 2022). Moreover, Xie et al. (2009) reported that reduction Availability of data and materials The datasets generated and/or analyzed during the current study are available of root activity in Deyeuxia angustifolia (Komarov) Y. L. in the Zenodo repository (Li et al. 2023) at https:// doi. org/ 10. 5281/ zenodo. Chang under waterlogging stress can be compensated for 75836 96. by high total root length. In turn we believe that loss of adventitious roots was compensated by increased primary Declarations root activity in S. nervosum. This speculation has been Ethics approval and consent to participate indirectly confirmed by Li et al. (2022b), who found that The authors declare that the study was not conducted on endangered, vulner- an increase in adventitious root activity in C. operculatus able or threatened species. [= S. nervosum] and S. cumini, with a partially damaged Consent for publication adventitious root system, contributes to water and nutri- The authors read and approved the final manuscript. ent transport under combined waterlogging and nutrient supply conditions. Consequently, although adventitious Competing interests The authors declare that they have no competing interests. root removal was detrimental to the growth of both spe- cies, S. nervosum showed less damage than S. cumini due Author details to the compensatory response of physiology and primary School of Ecological and Environmental Sciences, Hainan University, Hai- kou 570228, China. School of Life Sciences, Hainan University, Haikou 570228, roots. China. School of Plant Protection, Hainan University, Haikou 570228, China. Key Laboratory of Agro-Forestry Environmental Processes and Ecological 5 Conclusions and future perspectives Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of Hainan Province, Haikou 570228, China. We found that adventitious roots did not prevent injury to the growth of both species when primary roots Received: 11 October 2022 Accepted: 2 February 2023 were waterlogged, but species with a high proportion of adventitious roots would be at an advantage during waterlogging. 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Journal
Annals of Forest Science – Springer Journals
Published: Mar 7, 2023
Keywords: Adventitious roots removal; Compensatory response; Root system development; Waterlogging