Response of Chinese sea buckthorn clonal growth and photosynthetic physiological mechanisms toward a soil moisture gradient
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iForest Research Article doi: 10.3832/ifor3564-014 vol. 14, pp. 337-343 Biogeosciences and Forestry Response of Chinese sea buckthorn clonal growth and photosynthetic physiological mechanisms toward a soil moisture gradient Shuangcheng Bai (1), Studies have reported on the regulation of clonal growth in Chinese sea buck- thorn in response to environmental resource availability, but these studies Kaihong Nie (1), have been limited to external mechanisms. In this report, we controlled irriga- Shengli Ji (1), tion to generate a soil moisture gradient in order to examine the photosyn- Shi Chen (1), thetic physiological mechanisms regulating clonal growth in this species. The Zengyu Yao (1-2), results indicated that as irrigation intensity increased, the soil water content increased vertically and tissue water content first increased and then de- Genqian Li (1), creased. Furthermore, Rubisco activase (RCA) and Mg-chelatase H subunit Cuiping Tang (3), (CHLH) gene expression levels, photosynthetic capacity (net photosynthetic Feng Guo (4) rate, transpiration rate, chlorophyll content, and stomatal conductance), and clonal growth (ramet growth, clonal proliferation, clonal propagation) all showed a quadratic parabolic change (i.e., first increasing and then decreas- ing). In addition, gene expression levels and tissue water content, photosyn- thetic capacity and gene expression levels, and clonal growth and photosyn- thetic capacity were all significantly positively correlated. When irrigation in- tensity (soil water content) is exceedingly low or high, the tissue water con- tent is also low, RCA and CHLH gene expression levels are low, photosynthetic capacity is weak, clonal growth ability is inhibited, and clonal growth layout tends toward the “guerrilla type.” This type manifests as fewer and smaller clonal daughter ramets that are sparsely distributed with reduced clonal organ extension ability and branching intensity. When irrigation intensity (soil water content) is moderate, the tissue water content, gene expression levels, and photosynthetic capacity is high, clonal growth ability is completely uninhib- ited, and the clonal growth layout tends toward the “aggregated type.” This type is associated with numerous large clonal daughter ramets that are densely distributed with high clonal organ extension ability and branching in- tensity. Therefore, as irrigation intensity continuously changes from inordi- nately low to moderate to exceedingly high, Chinese sea buckthorn regulates clonal growth by photosynthetic capacity through photosynthetic gene expres- sion. This results in a clonal growth layout continuum of “guerrilla-aggregated- (1) College of Forestry, Southwest guerrilla” that depends on irrigation intensity. Forestry University, Kunming Yunnan 650224 (China); (2) Key Laboratory of Forest Re- Keywords: Clonal Growth, Irrigation Intensity, Tissue Water Content, Photosyn- sources Conservation and Utilization in the thetic Genes, RCA and CHLH Gene Expression, Hippophae rhamnoides ssp. Southwest Mountains of China - Southwest sinensis, Mu Us Sandy Land Forestry University, Ministry of Education, Kunming (China); (3) Wanyuan Forestry Sci- ence and Technology Extension Center, Introduction pine (Pinus taeda), 139 genes were differen- Dazhou, Sichuan 635000 (China); (4) Qianxi- Clonal growth refers to the process of tially expressed in response to sprouting. nan Bouyei and Miao Nationality Autonomous asexual reproduction in plants to produce The functions of these genes included sub- Prefectures Bureau of Forestry, Xingyi, genetically identical, morphologically and stance metabolism, stress responses, Guizhou 562400 (China) physiologically independent or potentially growth and development, signal transduc- independent individuals for spatial expan- tion, and hormonal regulation (Liu et al. @ Zengyu Yao (z-yyao@hotmail.com) sion under natural conditions, such as in 2011). Genqian Li (15825290016@163.com) stoloniferous or rhizomatous plants (Taka- Individual morphological variation among hashi et al. 2011, Robledo-Arnuncio et al. populations may originate from genetic Received: Jun 25, 2020 - Accepted: May 19, 2014). Currently, research on clonal growth changes (Rana & Shirkot 2012). It is evident 2021 regulation is focused on external mecha- from this that studying the relationship be- nisms, such as the response of clonal tween internal changes and clonal growth Citation: Bai S, Nie K, Ji S, Chen S, Yao Z, Li growth to environmental resource avail- might aid in further understanding the in- G, Tang C, Guo F (2021). Response of Chinese ability or heterogeneity and its ecological ternal mechanisms of regulation, particu- sea buckthorn clonal growth and photo- adaptation significance (He et al. 2009, larly the material and energy basis by synthetic physiological mechanisms toward a Tang et al. 2010, Wang et al. 2012, Luo et al. which photosynthetic intensity determines soil moisture gradient. iForest 14: 337-343. – 2013, Yan et al. 2013). However, clonal clonal growth (Wang et al. 2016). At the doi: 10.3832/ifor3564-014 [online 2021-07- growth regulation in plants is a complex same time, plant photosynthesis is regu- 15] process, as internal changes are closely as- lated by genes. An example is ribulose-1,5- sociated with clonal growth regulation. Fol- bisphosphate carboxylase (EC 4.1.1.39 – Ru- Communicated by: Silvano Fares lowing the removal of top growth in the bisco), which is a key enzyme that partici- shortleaf pine (Pinus echinata) and lobolly pates in the first rate-limiting step of car- © SISEF https://iforest.sisef.org/ 337 iForest 14: 337-343
Bai S et al. - iForest 14: 337-343 bon assimilation (Jurczyk et al. 2015). The perspective (Li et al. 2010b, He et al. 2012, is 53.1%. The geomorphological characteris- iForest – Biogeosciences and Forestry activity status of Rubisco is regulated and Zeng et al. 2016, Cao et al. 2016), and the tics of the site include undulating dunes controlled by Rubisco activase (RCA). In photosynthetic physiological regulatory and continuous sand belts, and the area other words, Rubisco must undergo activa- mechanisms for clonal growth are not well has an altitude of 1303-1418 m a.s.l. The soil tion by the RCA gene to elicit its carboxy- understood. In contrast, research on the consists mainly of aeolian sandy soil and lase and oxygenase activity, thereby in- photosynthetic physiology of sea buck- saline-alkaline soil, which are nutrient-defi- creasing photosynthetic efficiency (Parry et thorn has focused on the response laws of cient and have poor water and nutrient re- al. 2013, Carmo-Silva et al. 2015). Con- photosynthetic physiology characteristics tention abilities. The zonal vegetation is versely, chlorophylls are major pigments by to water levels (Li et al. 2002), and there is semi-desert grassland which is floristically which photosynthetic plants absorb and a lack of analysis on the causal relationship composed of psammophytes, xerophytes, transfer light energy, and their biosynthet- between photosynthetic physiological salt- and alkali-tolerant plants, and meso- ic route is completed by magnesium che- characteristics and plant growth. In a pre- phytic meadows. The experiment was con- latases. Among magnesium chelatases, liminary research (Cao et al. 2016), the rela- ducted at the Research and Development Mg-chelatase H subunit (CHLH) is a func- tionship between clonal growth and irriga- Base of Dingbian Forestry Station, and the tional gene that regulates chlorophyll syn- tion intensity was studied with 2-year-old soil is artificially-leveled aeolian sandy soil. thesis (Papenbrock et al. 2000, Pontier et sea buckthorn, and it was found that the The Chinese sea buckthorn naturally al. 2007, Ren et al. 2011). Therefore, RCA optimal irrigation intensity was close to 6 grows on banks of rivers and lakes and in and CHLH play important roles in photosyn- times the local annual precipitation, which valleys in the research area, where the soils thesis. This solicits an assessment of the is the highest irrigation intensity employed furnish good water conditions. The identi- causal relationship between RCA and CHLH in that experiment. Therefore, the result cal one-year-old seeded seedlings were gene expression, photosynthetic physio- could not fully describe the response of used in this experiment. The experiment logical characteristics, and clonal growth. clonal growth to the irrigation from deficit began in 2011, and after three years of con- The Chinese sea buckthorn (Hippophae to balance to surplus. In our study, the irri- tinuous observation, the final survey and rhamnoides ssp. sinensis) is an important gation intensity was adjusted to 3, 6, and 9 measurement were conducted at the end versatile woody species used for afforesta- times the local annual precipitation, and of the experiment in 2013. tion in arid and semiarid regions in North- the experiment was carried out for 3 years. ern China. It is a classic clonal plant that Through regulating soil water content and Experimental design and setup propagates via suckers, exhibiting ex- tissue water content by irrigation, we in- A univariate regression design was em- tremely strong lateral root horizontal ex- vestigated the response of photosynthetic ployed, and different irrigation intensities tension and branching abilities, and gener- gene expression, photosynthetic physio- were applied by adjusting the irrigation pe- ating large amounts of sucker plants dur- logical characteristics, and clonal growth riod with a fixed flow rate to simulate a ing propagation. This not only provides ability towards a moisture gradient. The natural precipitation gradient. Based on vegetation cover for areas that are difficult causal relationships between photosyn- preliminary experimental results (Li et al. to afforest but also assists in the expansion thetic physiology and clonal growth were 2010b, Cao et al. 2016), three irrigation gra- of the forest edge and renewal of forest investigated as well. The aim was to reveal dients were set up in this study, which gaps, thereby maintaining population sta- the response laws of Chinese sea buck- were three, six, and nine times the mean bility and clonal persistence (Li et al. 2001, thorn clonal growth to irrigation intensity annual precipitation of the study site. 2004, 2010a, He et al. 2006, Guo et al. and its photosynthetic physiology regula- Flood irrigation from a well was carried out 2015). After the parental plant has died, its tory mechanisms. for 280, 560, or 840 sec for each irrigation clonal daughter ramets can continue to un- gradient with a runoff of 6 L sec -1 on the dergo asexual propagation (Li et al. 2001, Materials and methods dates of 5th, 10th, 15th, 20th, 25th, and 30th Takahashi et al. 2011, Robledo-Arnuncio et from May to August in 2011-2013, and a al. 2014, Guo et al. 2015). Therefore, its Study site and plant material non-irrigated group was used as a control. clonal attributes have conferred the Chi- The study site was located at Dingbian (Tab. 1). A randomized arrangement was nese sea buckthorn with the potential for County in Shaanxi province (north-central used for the field layout, with a plot area of forest formation from a single tree and China) at the southern edge of the Mu Us 3 × 10 m. Triplicates were set up, resulting long-living. However, large areas of artifi- Sandy Land. The geographical coordinates in a total of 12 plots. The ridges between cial forests have undergone premature of the site are 107° 15′ ~ 108° 22′ E, 36° 49′ ~ the plots had a width of 0.5 m and a height senescence (Li et al. 2005, Hui et al. 2009). 37° 53′ N. The site has a mid-temperate arid of 0.3 m. Asphaltic felt and thick plastic The cause of this was determined to be and semiarid continental monsoon climate films were buried up to a depth of 1 m in drought stress, which weakens the clonal and experiences droughts and water short- the middle of the ridges for separation to growth abilities of Chinese sea buckthorn ages. The site has four distinct seasons, prevent water seepage. Thirty seedlings (Li et al. 2010b, He et al. 2012, Zhang et al.sufficient light, and frequent sandstorms. (one-year-old) were planted in every plot, 2016, Zeng et al. 2016, Cao et al. 2016). The annual mean temperature is 7.9 °C, with a distance of 1.0 × 1.5 m between the However, studies on the relationship be- mean annual precipitation is 316 mm and is seedlings. The two sides of every replicate tween soil moisture and clonal growth mostly concentrated in July to September, contained guard rows. have only explained the clonal growth reg- the annual evaporation amount is 2490 ulatory mechanisms from an ecological mm, and the annual mean relative humidity Experiment surveys and measurements All the measurements were conducted in Tab. 1 - Irrigation intensity design. (AvIR): average amount of irrigation per plot; 2013, the third year of the experiment. (EqPrec): Equivalent precipitation. Clonal growth parameters including ramet growth ability, clonal proliferation ability, and clonal propagation ability were mea- Moisture Treatment gradient AvIR EqPrec Irrigation Dates sured at the end of the growth phase in No. (kg yr-1) (mm) (May-August, 2011-2013) September (Li et al. 2001, 2004, 2010b, He (fold) et al. 2006, 2012, Guo et al. 2015, Cao et al. 1 0 - 300 Not irrigated 2016). For ramet (parent and daughter 2 3 40.500 900 5th, 10th, 15th, 20th, 25th, 30th ramet) growth ability, the amount of 3 6 81.000 1800 5th, 10th, 15th, 20th, 25th, 30th growth in tree height, base diameter, and 4 9 121.500 2700 th th th th th 5 , 10 , 15 , 20 , 25 , 30 th crown width were measured for every tree. For clonal proliferation ability, the 338 iForest 14: 337-343
Responses of sea buckthorn to irrigation iForest – Biogeosciences and Forestry Fig. 1 - Results of the regression analysis of (a) soil water content and (b) tissue water content to irrigation intensity, as well as of (c) tissue water content to soil water content (for more details, see Experiment Surveys and Measurements section). number of individuals was measured, i.e., for Chinese sea buckthorn. Three fully-ex- flection point for the regression formula the number of individual clonal (sprout) panded leaves with different orientations represents the optimal irrigation intensity daughter ramets in every experimental were selected from average standard (or soil water content) when the tissue wa- plot was tallied. The “tracking and digging” plants in every plot. ter content is the highest and values great- method was used for measuring clonal Twenty-four hours after irrigation, 5 g of er or lower than the optimal irrigation in- propagation ability, i.e., starting from a pri- young leaves were sampled from the top tensity (or soil water content) will result in mary lateral root (from the parent plant) of of average standard plants for the gene ex- a reduction in tissue water content. This an average standard tree, we followed and pression analyses, then rapidly placed in shows that as irrigation intensity increases, excavated the connecting secondary lat- liquid nitrogen and transported back to the the soil water content increases vertically, eral roots (originating from the primary lat- laboratory for storage at -80 °C. In the lab- while tissue water content initially in- eral roots) and tertiary lateral roots (origi- oratory, the UNIQ-10 Pillar TRIzol™ total creases before decreasing. nating from the secondary lateral roots) RNA extraction kit (SK1321/SK1322 – and measured the thickness, length, and Thermo Fisher Scientific Inc., Waltham, MA, Responses of photosynthetic gene quantity of the primary lateral roots and USA) was used to extract total RNA. Fol- expression levels to moisture gradient the total number of lateral roots. Soil mois- lowing that, cDNA synthesis was carried As reported in Tab. 2, as irrigation inten- ture content and moisture content of out before real-time PCR was used to mea- sity (x) increases, RCA and CHLH gene ex- leaves, chlorophyll content, and photosyn- sure the relative amounts of the RCA and pression levels (y) exhibit a quadratic para- thetic physiological indexes were repeat- CHLH genes in the cDNA samples. bolic change of the downward opening. edly measured for three cycles, i.e., August The inflection point of the formula repre- 16th-19th, 21st-24th, and 26th-29th. The mea- Data analysis sents the optimal irrigation intensity when surements were made from 8:00 to 20:00 All data were analyzed by regression anal- expression levels are the greatest, and val- every day. Net photosynthetic rate, tran- ysis and correlation analysis using the sta- ues greater or lower than the optimal irri- spiration rate, stomatal conductance were tistical software SPSS® ver. 17.0 (IBM, Ar- gation intensity will cause gene expression read at 2-hr intervals and other indicators monk, NY, USA). levels to decrease (similar to Fig. 1b). At the were measured at 4-hr intervals. The aver- same time, the variation trends in gene ex- ages of all the data in each cycle were pre- Results pression levels with increasing soil water sented as the final measured values. Soil content are consistent with the variation moisture content was measured with an Responses of soil and tissue water trends when irrigation intensity increases. ECH2O EC-5 dielectric water sensor (Dec- content to irrigation intensity However, gene expression levels and tis- agon Devices inc. Pullman, WA, USA) at From Fig. 1, it is evident that soil water sue water content (x) showed a significant fixed positions with depths of 10, 30, and content (y) and irrigation intensity (x) were positive correlation (similar to Fig. 1a). This 50 cm. Equal amounts (ca. 3.5 g) of leaves highly significantly positively correlated, indicates that the expression levels of RCA from the top, middle, and bottom of aver- while tissue water content (y) exhibit a and CHLH increase prior to decreasing as ir- age standard trees were collected and quadratic parabolic change of the down- rigation intensity (or soil water content) mixed for the tissue water content and ward opening with increasing irrigation in- and tissue water content increase. There- chlorophyll content tests. The tissue water tensity and soil water content (x). The in- fore, irrigation intensity (soil water con- content was determined by drying the specimen at 105 °C to constant weight, and then calculated from the formula: moisture Tab. 2 - Results of the regression analysis between gene expression parameters, irri- content (%) = 100 × (fresh mass – dry mass)/ gation intensity, and tissue water content. (R): correlation coefficient; (IP): equation fresh mass. Chlorophyll content was mea- inflection point. sured following the method in Li et al. (2010b). The LI-6800® Portable Photosyn- Regression thesis System (Li-Cor Environmental, Lin- Predictor (x) Regression equation R p-value IP variable (y) coln, NE, USA) was used to measure photo- Irrigation RCA y = -0.162x2 + 1.607x + 0.458 0.785 0.013 4.960 synthetic rate, transpiration rate, and Intensity CHLH y = -0.678x2 + 6.811x + 2.783 0.948
Bai S et al. - iForest 14: 337-343 iForest – Biogeosciences and Forestry Tab. 3 - Results of the regression analysis between photosynthesis physiological parameters, irrigation intensity, and tissue water content. (R): correlation coefficient; (IP): equation inflection point. Predictor (x) Regression variable (y) Regression equation R p-value IP Irrigation intensity Net photosynthetic rate y = -0.306x2 + 3.583x + 16.790 0.872 0.002 5.855 Transpiration rate y = -0.192x2 + 2.311x + 5.024 0.983
Responses of sea buckthorn to irrigation iForest – Biogeosciences and Forestry Tab. 6 - Correlation analysis between clonal growth and photosynthetic physiology parameters. (**): p
Bai S et al. - iForest 14: 337-343 reduced photosynthetic capacity during to the sandy nature of the soil which is References iForest – Biogeosciences and Forestry flag leaf senescence after the heading poor in water holding capacity. Cao ZL, Li TJ, Li GQ, Liu CH, Gao HY, Dai GH, Xiao stage in rice is intimately associated with ZY, Li SL (2016). Modular growth and clonal the decreased expression of Rubisco-acti- Conclusions propagation of Hippophae rhamnoides subsp. vating enzymes (RCA). Their study further In summary, irrigation intensity deter- sinensis in response to irrigation intensity. Jour- showed that initial Rubisco activity was mines soil water content, soil water con- nal of Forestry Research 27: 1019-1028. - doi: highly significantly positively correlated tent in turn determines tissue water con- 10.1007/s11676-016-0236-z with stomatal conductance and photosyn- tent, tissue water content in turn induces Carmo-Silva E, Scales JC, Madgwick PJ, Parry thetic rate. The activity of the Rubisco acti- changes in gene expression levels, gene MAJ (2015). Optimizing Rubisco and its regula- vating enzyme (RCA) is significantly posi- expression levels in turn regulate photo- tion for greater resource use efficiency. Plant tively correlated with transpiration rate synthetic capacity, and photosynthetic ca- Cell and Environment 38: 1817-1832. - doi: and photosynthetic rate (Weng et al. 2001). pacity in turn regulates clonal growth. This 10.1111/pce.12425 This study showed that net photosynthetic ultimately enables Chinese sea buckthorn Guo F, Tang CP, Xu DB, Li GQ, He B, Li TJ (2015). rate, transpiration rate, chlorophyll con- to form a clonal growth layout that is The edge dispersal regulation of the population tent, and stomatal conductance were sig- adapted to water resource availability. of clonal tree species Hippophae rhamnoides nificantly positively correlated with the ex- Specifically, when irrigation intensity (soil ssp. sinensis. Journal of Yunnan University (Nat- pression levels of RCA and CHLH, i.e., net water content) is low, the tissue water ural Science Edition) 37: 310-316. [in Chinese] - photosynthetic rate, transpiration rate, content will be low, RCA and CHLH gene ex- doi: 10.7540/j.ynu.20140275 chlorophyll content, and stomatal conduc- pression levels will be low, photosynthetic He B, Li GQ, Xu DB, Li TJ, Ni JP (2006). The clonal tance increase with increasing RCA and capacity will be weak, clonal growth ability growth and its ecological significance of Hip- CHLH expression levels. will be inhibited, and clonal growth layout pophae. Journal of Northwest Forestry Univer- Photosynthesis is the source of energy will tend toward “guerrilla type”. This type sity 21: 54-59. [in Chinese] - doi: 10.3969/j.issn. for plant growth and all metabolic activi- specifically manifests as fewer small daugh- 1001-7461.2006.03.014 ties (Wang et al. 2016). Our study found ter ramets that are sparsely distributed He B, Zhao FX, Li GQ, Ma XF, Xu DB, Li TJ (2012). that the growth, clonal proliferation, and with lower clonal organ extension ability The response of clonal growth of Hippophae clonal propagation abilities of Chinese sea and branching intensity. When irrigation in- rhamnoides L. subsp. sinensis to the availability buckthorn increase with increasing net tensity (soil water content) is moderate, of soil moisture in Mu Us Sandland. Journal of photosynthetic rate, transpiration rate, the tissue water content, gene expression Nanjing Forestry University (Natural Sciences chlorophyll content, and stomatal conduc- levels, and photosynthetic capacity will be Edition) 36: 46-50. [in Chinese] - doi: 10.3969/j.is tance. Conversely, Chinese sea buckthorn high, clonal growth ability will be uninhib- sn.1000-2006.2012.04.009 plants restricts photosynthetic physiology ited, and the clonal growth layout will tend He J, Zhao CJ, Qing H, Gan L, An SQ (2009). Ef- as a means of regulating clonal growth so toward the “aggregated type”. This type fect of soil water condition on morphological that clonal populations can adapt to the re- specifically manifests as numerous large plasticity of clonal plant Spartina alterniflora. source levels. This facilitates the complete daughter ramets that are densely distrib- Acta Ecologica Sinica 29: 3518-3524. [in Chi- utilization of environmental resources by uted with high clonal organ extension abil- nese] - doi: 10.3321/j.issn:1000-0933.2009.07.0 clones and increases population stability ity and branching intensity. When irrigation 09 (Li et al. 2010b, He et al. 2012, Zeng et al. intensity (soil water content) is exceed- Hui XX, Hong X, Yu X, Zhang LX (2009). Restora- 2016, Cao et al. 2016). When irrigation in- ingly high, RCA and CHLH gene expression tion of degraded Sea Buckthorn stands and tensity (soil water content) is suitable, levels will be low, photosynthetic capacity prospects in the Western Liaoning. The Global clonal growth layout tends toward the “ag- will be weak, clonal growth ability will be Seabuckthorn Research and Development 6: gregated type”. This not only facilitates en- inhibited, and clonal growth layout will 24-27. [in Chinese] - doi: 10.3969/j.issn.1672-483 vironmental resource occupation and uti- once again tend towards the “guerrilla 6.2009.04.005 lization by the population but also in- type”. Therefore, as irrigation intensity Jurczyk B, Hura K, Trzemecka A, Rapacz M creases the ability of the population to re- (soil water content) continuously changes (2015). Evidence for alternative splicing mecha- ject invasive species. When irrigation inten- from “overly low to moderate to overly nisms in meadow fescue (Festuca pratensis) sity (soil water content) is inordinately low high,” Chinese sea buckthorn restricts pho- and perennial ryegrass (Lolium perenne) Ru- or high, clonal growth layout tends toward tosynthetic physiology as a means of regu- bisco activase gene. Journal of Plant Physiology the “guerrilla type.” This allows the clones lating clonal growth in order for popula- 176: 61-64. - doi: 10.1016/j.jplph.2014.11.011 to search for environmental resources in a tions to form a clonal growth layout that Lawlor DW, Tezara W (2009). Causes of de- wider range and reduce competition be- adapts to water levels. This results in a creased photosynthetic rate and metabolic ca- tween clonal ramets. In addition, this in- clonal growth layout continuum of the pacity in water-deficient leaf cells: a critical creases the probability of clones placing “guerrilla-aggregated-guerrilla” type. evaluation of mechanisms and integration of ramets in a favorable habitat patch. How- processes. Annals of Botany 103: 561-579. - doi: ever, the tradeoffs include reduced ramet List of abbreviations 10.1093/aob/mcn244 growth, proliferation ability, and clonal The following abbreviations have been Li GQ, Huang BL, Tang DR, Zhao YQ, Wang DH propagation (Li et al. 2010b, He et al. 2012, used throughout the paper: RCA - Rubisco (2001). Regulation of clonal growth of Hip- Yan et al. 2013). Evidently, clonal growth activase; CHLH - Mg-chelatase H subunit. pophae rhamnoides L. subsp. sinensis popula- regulation is a manifestation of the ecologi- tion in Mu Us Sandland. Chinese Journal of Ap- cal adaptation countermeasures of Chinese Author Contribution plied Ecology 12: 682-686 [in Chinese] - doi: sea buckthorn populations and is a biologi- ScB and KhN contributed equally to this 10.13287/j.1001-9332.2001.0164 cal route for the maintenance of clonal per- paper (co-first authors). Li GQ, Zhao FX, Li XZ, Wei Y (2004). Density and sistence and population stability. biomass dynamics of Hippophae rhamnoides L. As suggested by our results in terms of Acknowledgments subsp. sinensis population in Mu Us Sandland. clonal growth, photosynthetic physiology, This work was supported by the National Scientia Silvae Sinicae 40: 180-184. [in Chinese] - and gene expression, both lower and Natural Science Foundation of China (Grant doi: 10.3321/j.issn:1001-7488.2004.01.030 higher irrigation intensities were unfavor- No. 31570609/31070551/30371193) and Sha- Li LX, Liang ZS, Han LR (2002). Effect of soil able to the plants. The former is obviously anxi Provincial Key Research and Develop- drought on the growth and water use efficien- attributed to drought. The latter might be ment Program (Grant No.2017ZDXM-NY- cy of Seabuckthorn. Acta Botanica Boreali-Occi- ascribed to waterlogging and leaching of 061). dentalia Sinica 22: 296-302. [in Chinese] - doi: soil nutrients. According to our observa- 10.3321/j.issn:1000-4025.2002.02.013 tion, the waterlogging was very short due Li Q, Zhang WH, He JF, Sun LL (2010a). Repro- 342 iForest 14: 337-343
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