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Chitosan Oligosaccharide Addition to Buddhist Pine (Podocarpus Macrophyllus (Thunb) Sweet) Under Drought: Reponses in Ecophysiology and Δ13c Abundance

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Chitosan Oligosaccharide Addition to Buddhist Pine (Podocarpus Macrophyllus (Thunb) Sweet) Under Drought: Reponses in Ecophysiology and Δ13c Abundance Article Chitosan Oligosaccharide Addition to Buddhist Pine (Podocarpus macrophyllus (Thunb) Sweet) under Drought: Reponses in Ecophysiology and δ13C Abundance Chunxia He 1,2, Yan Zhao 1,3, Jinsong Zhang 1,2 and Jun Gao 1,2,* 1 Key Laboratory of Tree Breeding and Cultivation of State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China; [email protected] (C.H.); [email protected] (Y.Z.); [email protected] (J.Z.) 2 Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China 3 Forestry college, Henan University of Science and Technology, Luoyang 471002, China * Correspondence: [email protected]; Tel./Fax: +86-10-6288-9636 Received: 13 April 2020; Accepted: 5 May 2020; Published: 8 May 2020 Abstract: Climate warming induces the necessity to increase the drought resistance of shade-obligate juvenile trees in sub-tropical forests. Chitosan oligosaccharide (COS) is a biopolymer derived from the marine resource that has attracted accumulative attention to induce and promote a plant’s resistance to abiotic stress. Buddhist pine (Podocarpus mascrophyllus (Thunb)Sweet) seedlings were cultured as the model material whose natural distribution in sub-tropical areas of China has suffered severe summer drought events in the last 113 years. A split-block design was conducted with a simulated drought event (drought vs. irrigated control), the COS addition, and two samplings at the ends of drought and re-watered treatments. The COS addition increased the resistance to drought by inducing a starch allocation towards roots where δ13C abundance and antioxidant enzyme activities were upregulated. The COS addition can promote biomass allocation to roots and increase the number of new roots. The COS addition to drought-treated Buddhist pine seedlings resulted in robust diameter growth. Therefore, COS is an available polymer to promote the resistance of Buddhist pine to drought. More work is suggested to clarify the dose of COS addition that can induce a prominent response of biomass accumulation and carbohydrate metabolism. Keywords: drought-resistance; soluble sugars; fine root morphology; seedling growth; biomass allocation; POD; SOD; CAT 1. Introduction Climate change brings about increasing drought events that shape the global forest distribution and changes the within-forest structure in all biomes [1]. Sub-tropical forests exchange more carbon dioxide (CO2) with the atmosphere than any other vegetation type; therefore, they are facing the most challenging droughts on the planet [2]. The pattern of precipitation shift exposes sub-tropical forests to foreseeing frequent drought events that may impair carbon (C) assimilation, even to the extent of vegetation dieback [3]. Facing frequent drought stresses, the functional composition of sub-tropical forests has been reformed from tall and strong dominant trees towards smaller and denser wooded dwarfs. During this process, the mortality of trees in sub-tropical forests has continuously occurred directly, or partially, due to water-deficit events. There is a large knowledge gap about the mechanism of drought-caused mortality in relation to sub-tropical forest trees [2,4]. People are helpless to cope with the drought impact on forest trees, even though it can be foreseen to come in high frequency. Forests 2020, 11, 526; doi:10.3390/f11050526 www.mdpi.com/journal/forests Forests 2020, 11, 526 2 of 13 The management and silvicultural practices are considered to adapt forests to drought under the guidance of a close-to-nature strategy. Density and diversity are two critical parameters that attract great attention considering modification towards a more drought-resistant forest ecosystem. Forests with a low tree population show solid adaptations to drought [5,6]. Sometimes heavy thinning management may be needed to remove as high as 60% of the basal area to promise the framework for the adaptation of forests to drought [6]. One of the most significant benefits of thinning is the creation of large gaps that promote undergrowth regeneration in forests exposed to a water-deficit condition [7]. Therefore, it is commonly suggested to bring more juvenile shade-tolerant trees to forest gaps to enhance the adaptation of the stand. The dependence on species screening will result in a low richness, which would, in turn, impact the sustainable development of the managed forest. An alternative approach is to improve the resistance to drought for newly introduced trees but, to our knowledge, no specific regime has been documented. Access to better adaptation appears to be enclosed if all strategies came only out of the approach derived from the terrestrial system. Our society is established on the terrestrial biota, but a highly developed economic industry brings about an increasing demand for the recycling utilization of marine resources [8]. Chitin is a type of cationic amino polysaccharide made up of N-acetyl D-glucosamine repeat blocks joined by β-1,4 glycosidic bonds [9]. Chitin is derived from leftover seafood by extraction from the exoskeletons of crustaceans and shrimp crabs [8]. To facilitate utilization, chitosan is usually converted into the most commonly known derivative of a linear heteropolysaccharide polycationic called “chitosan” [10]. Chitosan is a biopolymer of glucosamine residues that can also be processed from seafood wastes [11]. Chitosan oligosaccharide (oligochitosan or COS) is the enzymatic-hydrolyzed product of chitosan that overcomes the drawbacks of insolubility at neutral pH and high viscosity of chitosan [12]. As at least five acetyl groups have been found to be carried, COS has a valuable attribute to activate the plant immune system and promotes the generation of an anti-oxidative metabolism [13–15]. COS addition was also found to function as a growth modifier that induced biomass allocation to roots and strengthened nutrient uptake and utilization [11,16]. Recently, COS was found to promote plant resistance to drought stress through modification of plant morphological, physiological, and metabolic responses [17,18]. This implies COS to be a potential modifier that may bring drought resistance of juvenile trees in sub-tropical regions. The specific responses in ecophysiology need to be detected to reveal the solid mechanism for using COS. A non-structural carbohydrate (NSC; mainly soluble sugars and starch) metabolism is one of the earliest responses to drought stress as a link between responses of photosynthetic production and the subsequent utilization. NSC changes accompany the entire process of tree response to drought from growth deficit to essential mortality [19]. When facing a water-deficit event, both sugar and starch contents and partitioning in shoots are reduced due to the imposed impact on photosynthesis [20]. Starch is heavily consumed as hydrolyzing to sugars to fuel new root egress and elongation [21]. At the initial stage of root response to drought, the conversion from starch to sugars is stimulated for the supply of energy to fuel counter stress [22]. However, the heavy depletion of the starch reserve in roots exposed to drought can prevent the conversion to sugars, which primarily accounts for the mortality [23]. As a summary of the above-mentioned findings, NSC changes in response to the drought effect on both shoot and root parts can be taken as the scale to assess the effect of COS addition as a potential remission. A drought event induces the depression on leaves’ stomatal conductance (gs) to control transpiration; thereafter, intercellular CO2 (Ci/Ca) is stimulated to accumulate to a higher concentration, which arouses the increase of a C isotope signature (δ13C) in newly formed photosynthates. It was also found that δ13C declined in the fine roots of trees that were distributed in dry stands [24]. Recently evidence is still accumulating to employ δ13C as the indicator to assess trees’ response to drought interruption [25,26]. Therefore, the detection of δ13C can be a precise approach to quantify the effect of COS addition on the response of juvenile trees to drought. The activity of POD can assess the reactive oxygen species (ROS) scavenger, and active SOD rapidly converts the ROS into hydrogen peroxide and Forests 2020, 11, 526 3 of 13 water, which is catalyzed by CAT [14]. The activities of all these three enzymes are sensitive predictors of the antioxidant effect of COS addition on horticultural plants [27,28]. Therefore, they also have the full potential to be detected as an assessment for the anti-drought response of juvenile tree seedlings. Buddhist pine (Podocarpus mascrophyllus (Thunb) Sweet) is a widely distributed species in sub-tropical regions of Southern China that received the least concern by the Red List of International Union for Conservation of Nature (IUCN) [29]. The sub-tropical regions in Southern China are the main area of Buddhist pine distribution [29]. All these regions have experienced severe drought in July and August since 1960 [30]. As a well-adaptative species to these regions, Buddhist pine has generated a resistance to extreme drought that has not been revealed well. It is a proper species that is further used to detect the response of COS addition under drought. In this study, a simulated drought was enforced on Buddhist pine seedlings with the hypotheses that (i) the decline in growth and photosynthetic products in drought-treated seedlings can be alleviated by COS addition but (ii) δ13C would decline with COS addition in response
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