Clonal integration of stress signal induces morphological and physiological response of root within clonal network

Su-Juan Duan; Jie Du; Dong-Wei Yu; Xiang-Jun Pei; Da-Qiu Yin; Shi-Jun Wang; Qi-Zhong Tao; Yi Dan; Xiao-Chao Zhang; Jie Deng; Jin-Song Chen; Qing Wei; Ning-Fei Lei

doi:10.1371/journal.pone.0298258

Abstract

Clonal integration of defense or stress signal induced systemic resistance in leaf of interconnected ramets. However, similar effects of stress signal in root are poorly understood within clonal network. Clonal fragments of Centella asiaticas with first-young, second-mature, third-old and fourth-oldest ramets were used to investigate transportation or sharing of stress signal among interconnected ramets suffering from low water availability. Compared with control, oxidative stress in root of the first-young, second-mature and third-old ramets was significantly alleviated by exogenous ABA application to the fourth-oldest ramets as well as enhancement of antioxidant enzyme (SOD, POD, CAT and APX) activities and osmoregulation ability. Surface area and volume in root of the first-young ramets were significantly increased and total length in root of the third-old ramets was significantly decreased. POD activity in root of the fourth-oldest and third-old ramets was significantly enhanced by exogenous ABA application to the first-young ramets. Meanwhile, total length and surface area in root of the fourth-oldest and third-old ramets were significantly decreased. Ratio of belowground to aboveground biomass in the whole clonal fragments was significantly increased by exogenous ABA application to the fourth-oldest or first-young ramets. It is suggested that transportation or sharing of stress signal may induce systemic resistance in root of interconnected ramets. Specially, transportation or sharing of stress signal against phloem flow was observed in the experiment. Possible explanation is that rapid recovery of foliar photosynthesis in first-young ramets subjected to exogenous ABA application can partially reverse phloem flow within clonal network. Thus, our experiment provides insight into ecological implication on clonal integration of stress signal.

Citation: Duan S-J, Du J, Yu D-W, Pei X-J, Yin D-Q, Wang S-J, et al. (2024) Clonal integration of stress signal induces morphological and physiological response of root within clonal network. PLoS ONE 19(3): e0298258. https://doi.org/10.1371/journal.pone.0298258

Editor: Muhammad Jamil, Kohat University of Science and Technology, PAKISTAN

Received: December 29, 2022; Accepted: January 22, 2024; Published: March 6, 2024

Copyright: © 2024 Duan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This research was supported by Specialized Fund for the Post-Disaster Reconstruction and Heritage Protection in Sichuan Province (No.5132202019000128), Study and Application of Ecological Restoration Technology System for Wound Surface in the Middle Reaches of Yajiang River (JC2020/D02) and Study on Soil Maturation and Vegetation Reconstruction Technology of Large-Scale Spoil Soil Dump in Sichuan-Tibet Railway Construction (SKLGP2021Z07). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Clonal plants often propagate genetically identical ramets connected by spacer (stolon or rhizome) [1–3]. Resource substance (such as carbohydrates, nutrient and water) can be transported and shared among interconnected ramets, which is named as clonal integration [4–6]. So clonal integration may be very important for clonal plant, by provisioning internal support to ramets growing in patches of low resource availability or stressed environment [7–9].

Based on vascular connection such as stolon or rhizome, non-resource substance (such as defense signal) was transported or shared among interconnected ramets as well as resource substance [10–12]. With decrease of soluble carbohydrate content and change of phenolic composition, leaf strength and thickness of undamaged ramets were significantly increased by clonal integration of defense signal when interconnected ramets of stoloniferous herb Trifolium repens were subjected to herbivory damage from caterpillar Spodoptera exigua [13]. With increase of condensed tannin content, herbivory damage to leaf of young ramets was significantly alleviated by clonal integration of defense signal when jasmonic-acid was applied to the interconnected oldest ramets of rhizomatous sedge Carex alrofusca [14]. According to a risk-spreading strategy, systematic defense induced by clonal integration equalized herbivory preference and avoided selective feeding on young plant tissues [15]. With increase of antioxidant enzyme (SOD, POD, CAT and APX) activities, oxidative stress (O₂^•− production rate and malondialdehyde content) in the leaf of the old, mature and young ramets was significantly alleviated by exogenous ABA application to the oldest ramets of stoloniferous herb Centella asiaticas subjected to low water availability [16]. Generally, clonal integration of defense or stress signal may be dependent on phloem flow driven by source-sink relationship [16–18].

Abscisic acid plays an very important role in the plant response to water deficit [19]. Exogenous ABA application improved leaf photosynthetic rate and water use efficiency when the soybean was subjected to water deficit [20]. With exogenous ABA application, endogenous proline levels, chlorophyll, carotenoid, total carbohydrate contents, acid phosphatase and peroxidase were significantly increased when the Pisum sativum was subjected to water deficit [21]. To our knowledge, previous studies focused on foliar response of interconnected ramets induced by clonal integration of defense or stress signal. However, effects of transportation or sharing of defense or stress signal in root are poorly understood within clonal network. A pot experiment was conducted to investigate clonal integration of stress signal and its effects on morphological and physiological traits of root within clonal network.

As a perennial medicinal plant, Centella asiatica contain asiaticoside, madecasosside, asiatic acid and madecassic acid [22]. Clonal fragments of Centella asiatica first-young, second-mature, third-old, and fourth-oldest were suffering from low water availability (20% soil moisture content). Meanwhile, 5 mL ABA solution (0.1 mM) or same volume distilled water was applied to the first-young or fourth-oldest ramets respectively. Comparing with control (same volume distilled water treatment), we predicted that: (1) with increase of antioxidant enzyme (SOD, POD, CAT and APX) activities, oxidative stress (O₂^•− production rate and H₂O₂ content) in root of the first-young, second-mature and third-old ramets was significantly alleviated by exogenous ABA application to the fourth-oldest ramets; (2) proline (pro) and soluble protein content in root of the first-young, second-mature and third-old ramets were significantly increased by exogenous ABA application to the fourth-oldest ramets; (3) biomass accumulation and ratio of belowground to aboveground biomass in whole clonal fragment were significantly increased by exogenous ABA application to the fourth-oldest ramets; (4) total length, surface area and volume in root of the first-young, second-mature and third-old ramets were significantly greater when exogenous ABA was applied the fourth-oldest ramets.

Within clonal network, transportation or sharing of defense or stress signal can be dependent on phloem flow driven by source-sink relationship [17, 23]. Finally, we predicted that similar patterns were not observed in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

Materials and methods

Plant material

As a stoloniferous perennial herb, Centella asiatica (Umbelliferae) is distributed predominantly in woodlands, forests edges, damp grass, roadside or creek (about 200-1900m) [24]. Its stolon usually takes roots in contact with moist substratum, which forming a network of stolon above the ground. Each ramet of C. asiatica is consists of two zygomorphic leaves with slender petiole [25].

Seven original plants of C. asiatica were collected in Chengdu, Sichuan Province, China (30°05′-31°260N; 102°540–104°53°E). The original plants were away from at least 1 km. They were cultivated in a greenhouse with a 12/12 h day: night cycle at 27°C/22°C, located in Sichuan Normal University. After 4 months, clonal fragments of C. asiatica with first-young, second-mature, third-old, and fourth-oldest were selected. The clonal fragments were subjected to low water availability (20% volumetric soil moisture content).

Experimental design

5 mL ABA solution (0.1 mM) was applied to leaves of the first-young or fourth-oldest ramets respectively (Fig 1). As control, same volume distilled water was used [26]. Then, the first-young or fourth-oldest ramets respectively were sealed in transparent plastic bag until dry. The experiment lasted for 30 days. Each treatment was replicated 7 times.

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Fig 1. Schematic representation of the experimental design.

(a): 5 mL ABA solution (0.1 mM) was applied to the fourth-oldest ramets; (b): 5 mL ABA solution (0.1 mM) was applied to first-young ramets. Same volume distilled water was employed as control.

https://doi.org/10.1371/journal.pone.0298258.g001

Measurement of antioxidant enzyme activities, oxidative stress and osmoregulation ability.

UV-spectrophotometer was used to test antioxidant enzyme (SOD, POD, CAT and APX) activities, oxidative stress (O₂^•− production rate and H₂O₂ content) and osmoregulation ability (proline content and total soluble protein content) in root of the interconnected ramets [27–30].

Measurement of morphological characteristics.

WinRHIZO was used to measure total length, surface area and volume in root of the interconnected ramets [31].

Measurement of biomass accumulation and allocation.

After oven-dried at 70°C for 72 h, each clonal fragment was separated into root, leaf and stolon to weigh. Ratio of belowground to aboveground biomass was counted [32].

Statistical analysis

Two-way analysis of variance (ANOVA) was used to investigate the effects of exogenous ABA application, ramet age and their interaction on oxidative stress (O₂^•− production rate and H₂O₂ content), antioxidant enzyme (SOD, POD, CAT and APX) activities, osmoregulation ability (proline and soluble protein content) and morphological characteristics (total length, surface area and volume) in root of the interconnected ramets when exogenous ABA was applied to the first-young or fourth-oldest ramets respectively [33].

One-way analysis of variance (ANOVA) was employed to investigate effects of exogenous ABA application on biomass accumulation and allocation of whole clonal fragment [34].

Pearson’s correlation coefficient was employed to investigate correlation between oxidative stress (O₂^•− production rate and H₂O₂ content) and antioxidant capacity (SOD, POD, CAT and APX activities) [35]. Significance was set at the P ≤ 0.05 level. All analyses were conducted with SPSS 21.0 software (SPSS Inc.).

Results

Oxidative stress in root of the interconnected ramets

O₂^•− production rate and H₂O₂ content in root of the first-young, second-mature and third-old ramets significantly decreased when exogenous ABA was applied to the fourth-oldest ramets (Table 1, Fig 2A and 2B). At the same time, H₂O₂ content in root of the first-young and second-mature ramets significantly decreased than those in root of the third-old ramets (Table 1, Fig 2A and 2B).

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Fig 2. Oxidative stress in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the fourth-oldest ramets.

(a): O₂^•− production rate (mean ± SE); (b): H₂O₂ content (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g002

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Table 1. Effects of exogenous ABA application, ramet age and their interaction on oxidative stress (O2•− production rate and H₂O₂ content), antioxidant capacity (SOD, POD, CAT and APX activities), osmoregulation ability (Proline and soluble protein content), and morphological characteristics (total length, surface area and volume) in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the fourth-oldest ramets.

https://doi.org/10.1371/journal.pone.0298258.t001

In addition, O₂^•− production rate and H₂O₂ content in root of the second-mature, third-old and fourth-oldest ramets were not significantly affected by exogenous ABA application, ramet age and their interaction when exogenous ABA was applied to the first-young ramets (Table 2, Fig 3A and 3B).

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Fig 3. Oxidative stress in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

(a): O₂^•− production rate (mean ± SE); (b): H₂O₂ content (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g003

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Table 2. Effects of exogenous ABA application, ramet age and their interaction on oxidative stress (O2•− production rate and H₂O₂ content), antioxidant capacity (SOD, POD, CAT and APX activities), osmoregulation ability (Proline and soluble protein content), and morphological characteristics (total length, surface area and volume) in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

https://doi.org/10.1371/journal.pone.0298258.t002

Antioxidant enzyme activities in root of the interconnected ramets

CAT, POD, SOD and APX activities in root of the first-young, second-mature and third-old ramets significantly increased when exogenous ABA was applied to the fourth-oldest ramets (Table 1, Fig 4A–4D). Especially, POD, CAT and APX activities in root of the first-young ramets were significantly greater than those in the root of the second-mature and third-old ramets (Table 1, Fig 4A, 4B and 4D).

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Fig 4. Antioxidant enzyme activities in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the first-young ramets.

(a): superoxide dismutase (SOD) (mean ± SE); (b): peroxidase (POD) (mean ± SE); (c): catalase (CAT) (mean ± SE); (d): ascorbate peroxidase (APX) (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g004

Significantly positive correlation was found among the CAT, POD, SOD and APX activities in root of the interconnected ramets when exogenous ABA was applied to the fourth-oldest ramets (Table 3). Significantly negative correlation was found between H₂O₂ content and antioxidant enzyme (CAT, POD, SOD and APX) activities (Table 3). Similar pattern was not observed between O₂^•− production rate and antioxidant enzyme (CAT, POD, SOD and APX) activities (Table 3).

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Table 3. Correlation between oxidative stress (O2•− production rate and H₂O₂ content) and antioxidant capacity (SOD, POD, CAT and APX activities), in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the fourth-oldest ramets.

https://doi.org/10.1371/journal.pone.0298258.t003

POD activity in root of the third-old and fourth-oldest ramets significantly increased except for that in root of the second-mature ramets when exogenous ABA was applied to the first-young ramets (Table 2, Fig 5B). At the same time, SOD activity in root of the second-mature ramets and third-old ramets significantly increased than those in root of the fourth-oldest ramets (Table 2, Fig 5C). APX activity in root of the second-mature ramets significantly increased than those in root of the third-old and fourth-oldest ramets (Table 2, Fig 5D).

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Fig 5. Antioxidant enzyme activities in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

(a): superoxide dismutase (SOD) (mean ± SE); (b): peroxidase (POD) (mean ± SE); (c): catalase (CAT) (mean ± SE); (d): ascorbate peroxidase (APX) (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g005

CAT activity showed a positive and significant correlation with POD activity, whilst non-significant association with SOD and APX activities when exogenous ABA was applied to the first-young ramets (Table 4). At the same time, POD activity showed a positive and significant correlation with SOD activity, whilst non-significant association with APX activity (Table 4). SOD activity showed a positive but non-significant association with APX activity (Table 4). O₂^•− production rate showed a negative and significant correlation with SOD activity, whilst non-significant association with CAT, POD and APX activities (Table 4). H₂O₂ content showed a negative and significant correlation with O₂^•− production rate, whilst non-significant association with CAT, POD and APX activities (Table 4).

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Table 4. Correlation between oxidative stress (O2•− production rate and H₂O₂ content) and antioxidant capacity (SOD, POD, CAT and APX activities), in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

https://doi.org/10.1371/journal.pone.0298258.t004

Osmoregulation ability in root of the interconnected ramets

Proline and soluble protein contents in root of the first-young, second-mature and third-old ramets significantly increased when exogenous ABA was applied to the fourth-oldest ramets (Table 1, Fig 6A and 6B).

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Fig 6. Osmoregulation ability in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the fourth-oldest ramets.

(a): proline (Pro) content (mean ± SE); (b): soluble protein content (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g006

Proline content in root of the second-mature, third-old and fourth-oldest ramets were not significantly effects by exogenous ABA application to the first-young ramets (Table 2, Fig 7A). In addition, soluble protein content in root of the third-old ramets significantly increased with decrease of second-mature rements when exogenous ABA was applied to the first-young ramets (Table 2, Fig 7B). Meanwhile, proline and soluble protein content in root of the second-mature ramets were lower than those of the third-old and fourth-oldest ramets (Table 2, Fig 7A and 7B).

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Fig 7. Osmoregulation ability in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

(a): proline (Pro) content (mean ± SE); (b): soluble protein content (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g007

Morphological plasticity in root of the interconnected ramets

Total length in root of the third-old ramets significantly decreased with increase of surface area and volume in root of the first-young when exogenous ABA was applied to the fourth-oldest ramets (Table 1, Fig 8A–8C).

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Fig 8. Morphological plasticity in root of the first-young, second-mature and third-old ramets when exogenous ABA was applied to the fourth-oldest ramets.

(a): total length (mean ± SE); (b): surface area (mean ± SE); (c): volume (mean ± SE); Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g008

Total length and surface area in root of the fourth-oldest and third-old ramets significantly decreased when exogenous ABA was applied to the first-young ramets (Table 2, Fig 9A and 9B). Meanwhile, volume in root of the fourth-oldest ramets was greater than that in root of the second-mature ramets (Table 2, Fig 9C).

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Fig 9. Morphological plasticity in root of the second-mature, third-old and fourth-oldest ramets when exogenous ABA was applied to the first-young ramets.

(a): total length (mean ± SE); (b): surface area (mean ± SE); (c): volume (mean ± SE); Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g009

Biomass accumulation and allocation in the whole clonal fragment

Biomass accumulation and ratio of belowground to aboveground biomass in the whole clonal fragments significantly increased when exogenous ABA was applied to the fourth-oldest ramets (Fig 10A and 10B). Ratio of belowground to aboveground biomass in the whole clonal fragment significantly increased except for biomass accumulation when exogenous ABA was applied to the first-young ramets (Fig 11A and 11B).

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Fig 10. Biomass accumulation and allocation in the whole clonal fragments when exogenous ABA was applied to the fourth-oldest ramets.

(a): biomass accumulation (mean ± SE), (b): ratio of belowground to aboveground biomass (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g010

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Fig 11. Biomass accumulation and allocation in the whole clonal fragments when exogenous ABA was applied to the first-young ramets.

(a): biomass accumulation (mean ± SE), (b): ratio of belowground to aboveground biomass (mean ± SE). Open bar: control; closed bar: exogenous ABA application. Bars with the same lower case letters are not significantly different (P > 0.05).

https://doi.org/10.1371/journal.pone.0298258.g011

In the experiment, oxidative stress in root of interconnected ramets was alleviated by increase of antioxidant enzyme activity after local exogenous ABA application (Tables 1–4, Figs 2–7). Meanwhile, change of root morphology and biomass allocation of whole clonal fragments subjected to low water availability were responsible for improving of their growth performance (Tables 1 and 2, Figs 8–11).

Discussion

Exogenous ABA (60μM) application induced enhancement of foliar antioxidant enzyme activities (such as SOD, POD, APX, CAT) in kiwifruit subjected to drought stress, which alleviated oxidative stress (decrease of MDA and H₂O₂ content) in its leaf [36]. In addition, exogenous ABA application enhanced osmoregulation ability (increase of proline accumulation) in leaf of turgid barley seedlings (Hordeum rulgare var Larker) [37]. In the experiment, root systemic resistance (such as antioxidant enzyme activities and osmoregulation ability) induced by local exogenous ABA application, thereby improving growth performance of whole clonal fragments. Meanwhile, negative correlation between antioxidant enzyme (SOD, POD, CAT and APX) activities and H₂O₂ content in root of the first-young, second-mature and third-old ramets was observed when exogenous ABA was applied to the fourth-oldest ramets. The oxidative damage (such as H₂O₂) of the clonal fragments subjected to drought stress was alleviated by increase of antioxidant enzyme activity such as superoxide dismutase (SOD), catalase (CAT), peroxidases (POD), and ascorbate peroxidase (APX) [16, 38, 39].

Their root growth such as more lateral roots, greater primary root and total root length was improved when wild-type tomato (Solanum lycopersicum L) seedlings were suffering from severe drying [40]. Meanwhile, primary root growth in Arachis hypogaea, Arabidopsis and ‘Qingzhen 1’ apple seedlings was inhibited by exogenous ABA application [41–44]. In the experiment, local exogenous ABA application to the fourth-oldest ramets resulted in significant increase of surface area and volume in root of the first-young ramets as well as decrease of total length in root of the third-old ramets. The comprehensive effect between exogenous ABA application and drought stress on root growth may explain the above phenomena. Further, more studies are needed.

Defensive signal driven by phloem flow within clonal network mainly directed towards the acropetal direction [45, 46]. Transportation or sharing of defense signal against phloem flow was detected when the old ramets were subjected to shading within clonal network [17]. Meanwhile, transportation or sharing of stress signal against phloem flow within clonal network was observed in the experiment. Compared to PEG stress (15% polyethylene glycol), net photosynthetic rate in upland rice (resistant to drought stress) and lowland rice (susceptible to drought stress) seedlings experiencing PEG-stress was significantly increased after 48 h of exogenous ABA treatment. [47]. Thus, we tentatively concluded that rapid recovery of foliar photosynthesis could partially reverse phloem flow within clonal network when exogenous ABA was applied to the first-young ramets.

Transportation or sharing of biotic and abiotic stress signal within clonal network may be very important for survival and growth of clonal plants grown in unfavourable habitat [48, 49]. Systemic resistance and root growth stimulated by transportation or sharing of stress signal in root, thereby improving growth performance of whole clonal fragments subjected to low water availability [50]. Thus, our experiment provides insight into ecological implication on clonal integration of stress signal. Further studies are needed to understand the generality of this pattern and to assess fully the ecological advantages afforded by these features.

Supporting information

S1 Data.

https://doi.org/10.1371/journal.pone.0298258.s001

(XLSX)

References

1. Lin HF, Alpert P, Zhang Q, Yu FH. Facilitation of amphibious habit by physiological integration in the clonal, perennial, climbing herb Ipomoea aquatica. Science of The Total Environment. 2018; 618:262–268. pmid:29128776
- View Article
- PubMed/NCBI
- Google Scholar
2. Gao FL, Alpert P, Yu FH. Parasitism induces negative effects of physiological integration in a clonal plant. New Phytologist. 2021; 229(1):585–592. pmid:32846015
- View Article
- PubMed/NCBI
- Google Scholar
3. Dong BC, Alpert P, Zhang Q, Yu FH. Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia. 2015; 179(2):393–403. pmid:26009243
- View Article
- PubMed/NCBI
- Google Scholar
4. Wang JY, Xu TT, Wang Y, Li GG, Abdullah I, Zhong ZW, et al. A meta‐analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments. Functional Ecology. 2021;35(3):578–589. https://doi.org/10.1111/1365-2435.13732.
- View Article
- Google Scholar
5. Shi M, Zhang JB, Sun J, Li Q, Lin XC, Song xz. Unequal nitrogen translocation pattern caused by clonal integration between connected ramets ensures necessary nitrogen supply for young Moso bamboo growth. Environmental and Experimental Botany. 2022; 200:104900. https://doi.org/10.1016/j.envexpbot.2022.104900.
- View Article
- Google Scholar
6. Chen JS, Lei NF, Dong M. Clonal integration improves the tolerance of Carex praeclara to sand burial by compensatory response. Acta Oecologica. 2010; 36(1):23–28. https://doi.org/10.1016/j.actao.2009.09.006.
- View Article
- Google Scholar
7. Pu L, Cheng L, Li A, Liang S, Wei Q, Wu SL, et al. Effects of clonal integration on allelopathy of invasive plant Wedelia trilobata under heterogeneous light conditions. Journal of Plant Ecology. 2022; 15(3):663–671. https://doi.org/10.1093/jpe/rtab028.
- View Article
- Google Scholar
8. Shi JM, Mao SY, Wang LF, Ye XH, Wu J, Wang GR, et al. Clonal integration driven by source-sink relationships is constrained by rhizome branching architecture in a running bamboo species (Phyllostachys glauca): A 15N assessment in the field. Forest Ecology and Management. 2021; 481:118754. https://doi.org/10.1016/j.foreco.2020.118754.
- View Article
- Google Scholar
9. Reijers VC, Lammers C, de Rond AJA, Hoetjes SCS, Lamers LPM, van der Heide T. Resilience of beach grasses along a biogeomorphic successive gradient: resource availability vs. clonal integration. Oecologia. 2020; 192(1):201–212. pmid:31802199
- View Article
- PubMed/NCBI
- Google Scholar
10. Cope OL, Lindroth RL. Clonal Saplings of Trembling Aspen Do Not Coordinate Defense Induction. Journal of Chemical Ecology. 2018; 44(11):1045–1050. pmid:30109458
- View Article
- PubMed/NCBI
- Google Scholar
11. Jelinkova H, Tremblay F, Desrochers A. Herbivore-simulated induction of defenses in clonal networks of trembling aspen (Populus tremuloides). Tree Physiology. 2012; 32(11):1348–1356. pmid:23065192
- View Article
- PubMed/NCBI
- Google Scholar
12. Nihranz CT, Kolstrom RL, Kariyat RR, Mescher MC, De Moraes CM, Stephenson AG. Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae). Evolutionary Ecology. 2019; 33(4):499–520. https://doi.org/10.1007/s10682-019-09997-w.
- View Article
- Google Scholar
13. Gomez S, Onoda Y, Ossipov V, Stuefer JF. Systemic induced resistance: a risk-spreading strategy in clonal plant networks?. New Phytologist. 2008; 179(4):1142–1153. pmid:18627496
- View Article
- PubMed/NCBI
- Google Scholar
14. Chen JS, Lei NF, Liu Q. Defense signaling among interconnected ramets of a rhizomatous clonal plant, induced by jasmonic-acid application. Acta Oecologica. 2011; 37(4):355–360. https://doi.org/10.1016/j.actao.2011.04.002.
- View Article
- Google Scholar
15. Gomez S, Latzel V, Verhulst YM, Stuefer JF. Costs and benefits of induced resistance in a clonal plant network. Oecologia. 2007;153(4):921–930. pmid:17609982
- View Article
- PubMed/NCBI
- Google Scholar
16. Wei Q, Li Q, Jin Y, Wu SL, Fan LH, Lei NF, et al. Transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress. Funct Plant Biology. 2019; 46(7):613–623. https://doi.org/10.1071/FP18232.
- View Article
- Google Scholar
17. Gomez S, Stuefer, JF. Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia. 2006; 147(3): 461–468. https://doi.org/10.1007/s00442-005-0293-z.
- View Article
- Google Scholar
18. Touchette BW, Moody JWG, Byrne CM, Marcus SE. Water integration in the clonal emergent hydrophyte, Justicia americana: benefits of acropetal water transfer from mother to daughter ramets. Hydrobiologia. 2012; 702(1):83–94. https://doi.org/10.1007/s10750-012-1309-4.
- View Article
- Google Scholar
19. Salazar C, Hernandez C, Pino MT. Plant water stress: Associations between ethylene and abscisic acid response. Chilean journal of agricultural research. 2015; 75:71–79. https://doi.org/10.4067/s0718-58392015000300008.
- View Article
- Google Scholar
20. He J, Jin Y, Palta JA, Liu HY, Chen Z, Li FM. Exogenous ABA Induces Osmotic Adjustment, Improves Leaf Water Relations and Water Use Efficiency, But Not Yield in Soybean under Water Stress. Agronomy. 2019; 9(7):395. https://doi.org/10.3390/agronomy9070395.
- View Article
- Google Scholar
21. Latif HH. Physiological responses of Pisum sativum plant to exogenous ABA application under drought conditions. Pak J Bot. 2014; 46(3):973–982. https://doi.org/10.1007/s10725-010-9537-y.
- View Article
- Google Scholar
22. Bylka W, Znajdek-Awizen P, Studzinska-Sroka E, Danczak-Pazdrowska A, Brzezinska M. Centella asiatica in dermatology: an overview. Phytother Research. 2014; 28(8):1117–1124. pmid:24399761
- View Article
- PubMed/NCBI
- Google Scholar
23. Duchoslavová J, Weiser M. Evidence for unexpected higher benefits of clonal integration in nutrient-rich conditions. Folia Geobotanica. 2017; 52(3–4):283–294. https://doi.org/10.1007/s12224-016-9274-8.
- View Article
- Google Scholar
24. Li KN, Chen JS, Wei Q, Li Q, Lei NF. Effects of Transgenerational Plasticity on Morphological and Physiological Properties of Stoloniferous Herb Centella asiatica Subjected to High/Low Light. Front Plant Science. 2018; 9:1640. https://doi.org/10.3389/fpls.2018.01640.
- View Article
- Google Scholar
25. Nav SN, Ebrahimi SN, Sonboli A, Mirjalili M. Variability, association and path analysis of centellosides and agro-morphological characteristics in Iranian Centella asiatica (L.) Urban ecotypes. South African Journal of Botany. 2021; 139:254–266. https://doi.org/10.1016/j.sajb.2021.03.006.
- View Article
- Google Scholar
26. Dias MC, Correia C, Moutinho-Pereira J, Oliveira H, Santos C. Study of the effects of foliar application of ABA during acclimatization. Plant Cell, Tissue and Organ Culture (PCTOC). 2014; 117(2):213–224. https://doi.org/10.1007/s11240-014-0434-3.
- View Article
- Google Scholar
27. Li DX, Li CD, Sun HC, Wang WX, Liu LT, Zhang YJ. Effects of drought on soluble protein content and protective enzyme system in cotton leaves. Frontiers of Agriculture in China. 2010; 4(1):56–62. https://doi.org/10.1007/s11703-010-0102-2.
- View Article
- Google Scholar
28. Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and cell physiology. 1981; 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
- View Article
- Google Scholar
29. Menconi M, Sgherri CLM, Pinzino C, Navari-lzzo F. Activated oxygen production and detoxification in wheat plants subjected to a water deficit programme. Journal of Experimental Botany. 1995; 46(9):1123–1130. https://doi.org/10.1093/jxb/46.9.1123.
- View Article
- Google Scholar
30. Koca H, Bor M, Özdemir F, Türkan İ. The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environmental and Experimental Botany. 2007; 60(3):344–351. https://doi.org/10.1016/j.envexpbot.2006.12.005.
- View Article
- Google Scholar
31. Pornaro C, Macolino S, Menegon A, Richardson M. WinRHIZO Technology for Measuring Morphological Traits of Bermudagrass Stolons. Agronomy Journal. 2017; 109(6):3007–3010. https://doi.org/10.2134/agronj2017.03.0187.
- View Article
- Google Scholar
32. He LX, Xiao X, Zhang XM, Jin Y, Pu ZH, Lei NF, et al. Clonal fragments of stoloniferous invasive plants benefit more from stolon storage than their congeneric native species. Flora. 2021; 281:151877. https://doi.org/10.1016/j.flora.2021.151877.
- View Article
- Google Scholar
33. Corain L, Salmaso L. A Critical Review and a Comparative Study on Conditional Permutation Tests for Two-Way ANOVA. Communications in Statistics-Simulation and Computation. 2007; 36(4): 791–805. https://doi.org/10.1080/03610910701418119.
- View Article
- Google Scholar
34. Kim TK. Understanding one-way ANOVA using conceptual figures. Korean Journal of Anesthesiology. 2017; 70(1):22–26. pmid:28184262
- View Article
- PubMed/NCBI
- Google Scholar
35. Rehman A, Mustafa N, Du X, Azhar MT. Heritability and correlation analysis of morphological and yield traits in genetically modified cotton. Journal of Cotton Research. 2020;3(1):1–9. https://doi.org/10.1186/s42397-020-00067-z.
- View Article
- Google Scholar
36. Wang YL, Ma FW, Li MJ, Liang D, Zou J. Physiological responses of kiwifruit plants to exogenous ABA under drought conditions. Plant Growth Regulation. 2010; 64(1):63–74. https://doi.org/10.1007/s10725-010-9537-y.
- View Article
- Google Scholar
37. Stewart CR, Voetberg G. Relationship between Stress-Induced ABA and Proline Accumulations and ABA-Induced Proline Accumulation in Excised Barley Leaves. Plant Physiology. 1985; 79(1): 24–27. pmid:16664378
- View Article
- PubMed/NCBI
- Google Scholar
38. Zhang Y, Li Z, Peng Y, Wang XJ, Peng DD, He XS, et al. Clones of FeSOD, MDHAR, DHAR Genes from White Clover and Gene Expression Analysis of ROS-Scavenging Enzymes during Abiotic Stress and Hormone Treatments. Molecules. 2015; 20(11):20939–20954. pmid:26610459
- View Article
- PubMed/NCBI
- Google Scholar
39. Dou Y, Chang CM, Wang J, Cai ZP, Zhang W, Du HY, et al. Hydrogen Sulfide Inhibits Enzymatic Browning of Fresh-Cut Chinese Water Chestnuts. Frontiers in Nutrition. 2021; 8:652984. pmid:34150826
- View Article
- PubMed/NCBI
- Google Scholar
40. Zhang Q, Yuan W, Wang QW, Cao YY, Xu FY, Dodd IC, et al. ABA regulation of root growth during soil drying and recovery can involve auxin response. Plant, Cell & Environment. 2022; 45(3): 871–883. pmid:34176142
- View Article
- PubMed/NCBI
- Google Scholar
41. Smet ID, Signora L, Beeckman T, Inze´ D, Foyer CH, Zhang HM. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. The Plant Journal. 2003; 33(3):543–555. https://doi.org/10.1046/j.1365-313x.2003.01652.x
- View Article
- Google Scholar
42. Guo D, Liang J, Li L. Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regulation. 2009; 58(2): 173–179. https://doi.org/10.1007/s10725-009-9365-0.
- View Article
- Google Scholar
43. Sun LR, Wang YB, He SB, Hao FS. Mechanisms for Abscisic Acid Inhibition of Primary Root Growth. Plant Signal Behav. 2018; 13(9):e1500069. pmid:30081737
- View Article
- PubMed/NCBI
- Google Scholar
44. Zhang XY, Tahir MM, Li SH, Tang T, Mao JP,Li K, et al. Effect of Exogenous Abscisic acid (ABA) on the Morphology, Phytohormones, and Related Gene Expression of Developing Lateral Roots in ‘Qingzhen 1’. Plant Cell, Tissue and Organ Culture (PCTOC). 2021;148(1):23–24. https://doi.org/10.21203/rs.3.rs-670691/v1.
- View Article
- Google Scholar
45. Stuefer JF, Gómez S, Mölken Tv. Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evolutionary Ecology. 2005; 18(5–6):647–667. https://doi.org/10.1007/s10682-004-5148-2.
- View Article
- Google Scholar
46. Portela R, Barreiro R, Roiloa SR, Osborne B. Effects of resource sharing directionality on physiologically integrated clones of the invasive Carpobrotus edulis. Journal of Plant Ecology. 2021; 14(5): 884–895. https://doi.org/10.1093/jpe/rtab040.
- View Article
- Google Scholar
47. Teng KQ, Li JZ, Liu L, Han YC, Du YX, Zhang J, et al. Exogenous ABA induces drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiologiae Plantarum. 2014; 36(8):2219–2227. https://doi.org/10.1007/s11738-014-1599-4.
- View Article
- Google Scholar
48. Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD. Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytologist. 2014; 204(2):380–385. pmid:24920243
- View Article
- PubMed/NCBI
- Google Scholar
49. Sharifi R, Ryu CM. Social networking in crop plants: Wired and wireless cross-plant communications. Plant Cell Environment. 2021; 44(4):1095–1110. pmid:33274469
- View Article
- PubMed/NCBI
- Google Scholar
50. Roiloa SR, Antelo B, Retuerto R. Physiological integration modifies delta15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring. Annnals Botany. 2014; 114(2):399–411. https://doi.org/10.1093/aob/mcu064.
- View Article
- Google Scholar

[ref1] 1. Lin HF, Alpert P, Zhang Q, Yu FH. Facilitation of amphibious habit by physiological integration in the clonal, perennial, climbing herb Ipomoea aquatica. Science of The Total Environment. 2018; 618:262–268. pmid:29128776
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. Gao FL, Alpert P, Yu FH. Parasitism induces negative effects of physiological integration in a clonal plant. New Phytologist. 2021; 229(1):585–592. pmid:32846015
View Article
PubMed/NCBI
Google Scholar

[6] View Article

[7] PubMed/NCBI

[8] Google Scholar

[ref3] 3. Dong BC, Alpert P, Zhang Q, Yu FH. Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia. 2015; 179(2):393–403. pmid:26009243
View Article
PubMed/NCBI
Google Scholar

[10] View Article

[11] PubMed/NCBI

[12] Google Scholar

[ref4] 4. Wang JY, Xu TT, Wang Y, Li GG, Abdullah I, Zhong ZW, et al. A meta‐analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments. Functional Ecology. 2021;35(3):578–589. https://doi.org/10.1111/1365-2435.13732.
View Article
Google Scholar

[14] View Article

[15] Google Scholar

[ref5] 5. Shi M, Zhang JB, Sun J, Li Q, Lin XC, Song xz. Unequal nitrogen translocation pattern caused by clonal integration between connected ramets ensures necessary nitrogen supply for young Moso bamboo growth. Environmental and Experimental Botany. 2022; 200:104900. https://doi.org/10.1016/j.envexpbot.2022.104900.
View Article
Google Scholar

[17] View Article

[18] Google Scholar

[ref6] 6. Chen JS, Lei NF, Dong M. Clonal integration improves the tolerance of Carex praeclara to sand burial by compensatory response. Acta Oecologica. 2010; 36(1):23–28. https://doi.org/10.1016/j.actao.2009.09.006.
View Article
Google Scholar

[20] View Article

[21] Google Scholar

[ref7] 7. Pu L, Cheng L, Li A, Liang S, Wei Q, Wu SL, et al. Effects of clonal integration on allelopathy of invasive plant Wedelia trilobata under heterogeneous light conditions. Journal of Plant Ecology. 2022; 15(3):663–671. https://doi.org/10.1093/jpe/rtab028.
View Article
Google Scholar

[23] View Article

[24] Google Scholar

[ref8] 8. Shi JM, Mao SY, Wang LF, Ye XH, Wu J, Wang GR, et al. Clonal integration driven by source-sink relationships is constrained by rhizome branching architecture in a running bamboo species (Phyllostachys glauca): A 15N assessment in the field. Forest Ecology and Management. 2021; 481:118754. https://doi.org/10.1016/j.foreco.2020.118754.
View Article
Google Scholar

[26] View Article

[27] Google Scholar

[ref9] 9. Reijers VC, Lammers C, de Rond AJA, Hoetjes SCS, Lamers LPM, van der Heide T. Resilience of beach grasses along a biogeomorphic successive gradient: resource availability vs. clonal integration. Oecologia. 2020; 192(1):201–212. pmid:31802199
View Article
PubMed/NCBI
Google Scholar

[29] View Article

[30] PubMed/NCBI

[31] Google Scholar

[ref10] 10. Cope OL, Lindroth RL. Clonal Saplings of Trembling Aspen Do Not Coordinate Defense Induction. Journal of Chemical Ecology. 2018; 44(11):1045–1050. pmid:30109458
View Article
PubMed/NCBI
Google Scholar

[33] View Article

[34] PubMed/NCBI

[35] Google Scholar

[ref11] 11. Jelinkova H, Tremblay F, Desrochers A. Herbivore-simulated induction of defenses in clonal networks of trembling aspen (Populus tremuloides). Tree Physiology. 2012; 32(11):1348–1356. pmid:23065192
View Article
PubMed/NCBI
Google Scholar

[37] View Article

[38] PubMed/NCBI

[39] Google Scholar

[ref12] 12. Nihranz CT, Kolstrom RL, Kariyat RR, Mescher MC, De Moraes CM, Stephenson AG. Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae). Evolutionary Ecology. 2019; 33(4):499–520. https://doi.org/10.1007/s10682-019-09997-w.
View Article
Google Scholar

[41] View Article

[42] Google Scholar

[ref13] 13. Gomez S, Onoda Y, Ossipov V, Stuefer JF. Systemic induced resistance: a risk-spreading strategy in clonal plant networks?. New Phytologist. 2008; 179(4):1142–1153. pmid:18627496
View Article
PubMed/NCBI
Google Scholar

[44] View Article

[45] PubMed/NCBI

[46] Google Scholar

[ref14] 14. Chen JS, Lei NF, Liu Q. Defense signaling among interconnected ramets of a rhizomatous clonal plant, induced by jasmonic-acid application. Acta Oecologica. 2011; 37(4):355–360. https://doi.org/10.1016/j.actao.2011.04.002.
View Article
Google Scholar

[48] View Article

[49] Google Scholar

[ref15] 15. Gomez S, Latzel V, Verhulst YM, Stuefer JF. Costs and benefits of induced resistance in a clonal plant network. Oecologia. 2007;153(4):921–930. pmid:17609982
View Article
PubMed/NCBI
Google Scholar

[51] View Article

[52] PubMed/NCBI

[53] Google Scholar

[ref16] 16. Wei Q, Li Q, Jin Y, Wu SL, Fan LH, Lei NF, et al. Transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress. Funct Plant Biology. 2019; 46(7):613–623. https://doi.org/10.1071/FP18232.
View Article
Google Scholar

[55] View Article

[56] Google Scholar

[ref17] 17. Gomez S, Stuefer, JF. Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia. 2006; 147(3): 461–468. https://doi.org/10.1007/s00442-005-0293-z.
View Article
Google Scholar

[58] View Article

[59] Google Scholar

[ref18] 18. Touchette BW, Moody JWG, Byrne CM, Marcus SE. Water integration in the clonal emergent hydrophyte, Justicia americana: benefits of acropetal water transfer from mother to daughter ramets. Hydrobiologia. 2012; 702(1):83–94. https://doi.org/10.1007/s10750-012-1309-4.
View Article
Google Scholar

[61] View Article

[62] Google Scholar

[ref19] 19. Salazar C, Hernandez C, Pino MT. Plant water stress: Associations between ethylene and abscisic acid response. Chilean journal of agricultural research. 2015; 75:71–79. https://doi.org/10.4067/s0718-58392015000300008.
View Article
Google Scholar

[64] View Article

[65] Google Scholar

[ref20] 20. He J, Jin Y, Palta JA, Liu HY, Chen Z, Li FM. Exogenous ABA Induces Osmotic Adjustment, Improves Leaf Water Relations and Water Use Efficiency, But Not Yield in Soybean under Water Stress. Agronomy. 2019; 9(7):395. https://doi.org/10.3390/agronomy9070395.
View Article
Google Scholar

[67] View Article

[68] Google Scholar

[ref21] 21. Latif HH. Physiological responses of Pisum sativum plant to exogenous ABA application under drought conditions. Pak J Bot. 2014; 46(3):973–982. https://doi.org/10.1007/s10725-010-9537-y.
View Article
Google Scholar

[70] View Article

[71] Google Scholar

[ref22] 22. Bylka W, Znajdek-Awizen P, Studzinska-Sroka E, Danczak-Pazdrowska A, Brzezinska M. Centella asiatica in dermatology: an overview. Phytother Research. 2014; 28(8):1117–1124. pmid:24399761
View Article
PubMed/NCBI
Google Scholar

[73] View Article

[74] PubMed/NCBI

[75] Google Scholar

[ref23] 23. Duchoslavová J, Weiser M. Evidence for unexpected higher benefits of clonal integration in nutrient-rich conditions. Folia Geobotanica. 2017; 52(3–4):283–294. https://doi.org/10.1007/s12224-016-9274-8.
View Article
Google Scholar

[77] View Article

[78] Google Scholar

[ref24] 24. Li KN, Chen JS, Wei Q, Li Q, Lei NF. Effects of Transgenerational Plasticity on Morphological and Physiological Properties of Stoloniferous Herb Centella asiatica Subjected to High/Low Light. Front Plant Science. 2018; 9:1640. https://doi.org/10.3389/fpls.2018.01640.
View Article
Google Scholar

[80] View Article

[81] Google Scholar

[ref25] 25. Nav SN, Ebrahimi SN, Sonboli A, Mirjalili M. Variability, association and path analysis of centellosides and agro-morphological characteristics in Iranian Centella asiatica (L.) Urban ecotypes. South African Journal of Botany. 2021; 139:254–266. https://doi.org/10.1016/j.sajb.2021.03.006.
View Article
Google Scholar

[83] View Article

[84] Google Scholar

[ref26] 26. Dias MC, Correia C, Moutinho-Pereira J, Oliveira H, Santos C. Study of the effects of foliar application of ABA during acclimatization. Plant Cell, Tissue and Organ Culture (PCTOC). 2014; 117(2):213–224. https://doi.org/10.1007/s11240-014-0434-3.
View Article
Google Scholar

[86] View Article

[87] Google Scholar

[ref27] 27. Li DX, Li CD, Sun HC, Wang WX, Liu LT, Zhang YJ. Effects of drought on soluble protein content and protective enzyme system in cotton leaves. Frontiers of Agriculture in China. 2010; 4(1):56–62. https://doi.org/10.1007/s11703-010-0102-2.
View Article
Google Scholar

[89] View Article

[90] Google Scholar

[ref28] 28. Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and cell physiology. 1981; 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
View Article
Google Scholar

[92] View Article

[93] Google Scholar

[ref29] 29. Menconi M, Sgherri CLM, Pinzino C, Navari-lzzo F. Activated oxygen production and detoxification in wheat plants subjected to a water deficit programme. Journal of Experimental Botany. 1995; 46(9):1123–1130. https://doi.org/10.1093/jxb/46.9.1123.
View Article
Google Scholar

[95] View Article

[96] Google Scholar

[ref30] 30. Koca H, Bor M, Özdemir F, Türkan İ. The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environmental and Experimental Botany. 2007; 60(3):344–351. https://doi.org/10.1016/j.envexpbot.2006.12.005.
View Article
Google Scholar

[98] View Article

[99] Google Scholar

[ref31] 31. Pornaro C, Macolino S, Menegon A, Richardson M. WinRHIZO Technology for Measuring Morphological Traits of Bermudagrass Stolons. Agronomy Journal. 2017; 109(6):3007–3010. https://doi.org/10.2134/agronj2017.03.0187.
View Article
Google Scholar

[101] View Article

[102] Google Scholar

[ref32] 32. He LX, Xiao X, Zhang XM, Jin Y, Pu ZH, Lei NF, et al. Clonal fragments of stoloniferous invasive plants benefit more from stolon storage than their congeneric native species. Flora. 2021; 281:151877. https://doi.org/10.1016/j.flora.2021.151877.
View Article
Google Scholar

[104] View Article

[105] Google Scholar

[ref33] 33. Corain L, Salmaso L. A Critical Review and a Comparative Study on Conditional Permutation Tests for Two-Way ANOVA. Communications in Statistics-Simulation and Computation. 2007; 36(4): 791–805. https://doi.org/10.1080/03610910701418119.
View Article
Google Scholar

[107] View Article

[108] Google Scholar

[ref34] 34. Kim TK. Understanding one-way ANOVA using conceptual figures. Korean Journal of Anesthesiology. 2017; 70(1):22–26. pmid:28184262
View Article
PubMed/NCBI
Google Scholar

[110] View Article

[111] PubMed/NCBI

[112] Google Scholar

[ref35] 35. Rehman A, Mustafa N, Du X, Azhar MT. Heritability and correlation analysis of morphological and yield traits in genetically modified cotton. Journal of Cotton Research. 2020;3(1):1–9. https://doi.org/10.1186/s42397-020-00067-z.
View Article
Google Scholar

[114] View Article

[115] Google Scholar

[ref36] 36. Wang YL, Ma FW, Li MJ, Liang D, Zou J. Physiological responses of kiwifruit plants to exogenous ABA under drought conditions. Plant Growth Regulation. 2010; 64(1):63–74. https://doi.org/10.1007/s10725-010-9537-y.
View Article
Google Scholar

[117] View Article

[118] Google Scholar

[ref37] 37. Stewart CR, Voetberg G. Relationship between Stress-Induced ABA and Proline Accumulations and ABA-Induced Proline Accumulation in Excised Barley Leaves. Plant Physiology. 1985; 79(1): 24–27. pmid:16664378
View Article
PubMed/NCBI
Google Scholar

[120] View Article

[121] PubMed/NCBI

[122] Google Scholar

[ref38] 38. Zhang Y, Li Z, Peng Y, Wang XJ, Peng DD, He XS, et al. Clones of FeSOD, MDHAR, DHAR Genes from White Clover and Gene Expression Analysis of ROS-Scavenging Enzymes during Abiotic Stress and Hormone Treatments. Molecules. 2015; 20(11):20939–20954. pmid:26610459
View Article
PubMed/NCBI
Google Scholar

[124] View Article

[125] PubMed/NCBI

[126] Google Scholar

[ref39] 39. Dou Y, Chang CM, Wang J, Cai ZP, Zhang W, Du HY, et al. Hydrogen Sulfide Inhibits Enzymatic Browning of Fresh-Cut Chinese Water Chestnuts. Frontiers in Nutrition. 2021; 8:652984. pmid:34150826
View Article
PubMed/NCBI
Google Scholar

[128] View Article

[129] PubMed/NCBI

[130] Google Scholar

[ref40] 40. Zhang Q, Yuan W, Wang QW, Cao YY, Xu FY, Dodd IC, et al. ABA regulation of root growth during soil drying and recovery can involve auxin response. Plant, Cell & Environment. 2022; 45(3): 871–883. pmid:34176142
View Article
PubMed/NCBI
Google Scholar

[132] View Article

[133] PubMed/NCBI

[134] Google Scholar

[ref41] 41. Smet ID, Signora L, Beeckman T, Inze´ D, Foyer CH, Zhang HM. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. The Plant Journal. 2003; 33(3):543–555. https://doi.org/10.1046/j.1365-313x.2003.01652.x
View Article
Google Scholar

[136] View Article

[137] Google Scholar

[ref42] 42. Guo D, Liang J, Li L. Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regulation. 2009; 58(2): 173–179. https://doi.org/10.1007/s10725-009-9365-0.
View Article
Google Scholar

[139] View Article

[140] Google Scholar

[ref43] 43. Sun LR, Wang YB, He SB, Hao FS. Mechanisms for Abscisic Acid Inhibition of Primary Root Growth. Plant Signal Behav. 2018; 13(9):e1500069. pmid:30081737
View Article
PubMed/NCBI
Google Scholar

[142] View Article

[143] PubMed/NCBI

[144] Google Scholar

[ref44] 44. Zhang XY, Tahir MM, Li SH, Tang T, Mao JP,Li K, et al. Effect of Exogenous Abscisic acid (ABA) on the Morphology, Phytohormones, and Related Gene Expression of Developing Lateral Roots in ‘Qingzhen 1’. Plant Cell, Tissue and Organ Culture (PCTOC). 2021;148(1):23–24. https://doi.org/10.21203/rs.3.rs-670691/v1.
View Article
Google Scholar

[146] View Article

[147] Google Scholar

[ref45] 45. Stuefer JF, Gómez S, Mölken Tv. Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evolutionary Ecology. 2005; 18(5–6):647–667. https://doi.org/10.1007/s10682-004-5148-2.
View Article
Google Scholar

[149] View Article

[150] Google Scholar

[ref46] 46. Portela R, Barreiro R, Roiloa SR, Osborne B. Effects of resource sharing directionality on physiologically integrated clones of the invasive Carpobrotus edulis. Journal of Plant Ecology. 2021; 14(5): 884–895. https://doi.org/10.1093/jpe/rtab040.
View Article
Google Scholar

[152] View Article

[153] Google Scholar

[ref47] 47. Teng KQ, Li JZ, Liu L, Han YC, Du YX, Zhang J, et al. Exogenous ABA induces drought tolerance in upland rice: the role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiologiae Plantarum. 2014; 36(8):2219–2227. https://doi.org/10.1007/s11738-014-1599-4.
View Article
Google Scholar

[155] View Article

[156] Google Scholar

[ref48] 48. Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD. Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytologist. 2014; 204(2):380–385. pmid:24920243
View Article
PubMed/NCBI
Google Scholar

[158] View Article

[159] PubMed/NCBI

[160] Google Scholar

[ref49] 49. Sharifi R, Ryu CM. Social networking in crop plants: Wired and wireless cross-plant communications. Plant Cell Environment. 2021; 44(4):1095–1110. pmid:33274469
View Article
PubMed/NCBI
Google Scholar

[162] View Article

[163] PubMed/NCBI

[164] Google Scholar

[ref50] 50. Roiloa SR, Antelo B, Retuerto R. Physiological integration modifies delta15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring. Annnals Botany. 2014; 114(2):399–411. https://doi.org/10.1093/aob/mcu064.
View Article
Google Scholar

[166] View Article

[167] Google Scholar

Figures

Abstract

Introduction

Materials and methods

Plant material

Experimental design

Measurement of antioxidant enzyme activities, oxidative stress and osmoregulation ability.

Measurement of morphological characteristics.

Measurement of biomass accumulation and allocation.

Statistical analysis

Results

Oxidative stress in root of the interconnected ramets

Antioxidant enzyme activities in root of the interconnected ramets

Osmoregulation ability in root of the interconnected ramets

Morphological plasticity in root of the interconnected ramets

Biomass accumulation and allocation in the whole clonal fragment

Discussion

Supporting information

S1 Data.

References