Abstract
Leymus chinensis, a dominant species in the Songnen Plain of northeast China, has a strong ability to resist grazing and tolerate saline-alkali stress. Compensatory growth is a positive response of plants, when subjected to grazing or clipping stress; however, little information is available on how plant nitrogen allocation strategies affect compensatory growth under saline-alkali stress. A field experiment using two saline-alkali levels and three clipping levels was conducted in conjunction with the belowground 15N-urea labelling method. Irrespective of clipping and salt-alkali stress, moderate clipping significantly promoted allocation of newly-absorbed nitrogen (N) to shoots, resulting in high biomass and over-compensatory growth of L. chinensis. However, severe clipping dramatically decreased uptake of total 15N by 20% under saline-alkali conditions, resulting in under-compensatory growth, and plants allocated more N to stem bases than to other plant organs, showing a conservative N allocation strategy. Our results suggest that plants have different nitrogen allocation strategies under different combinations of environmental stresses.
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References
Alpert P (1999) Effects of clonal integration on plant plasticity in Fragaria chiloensis. Plant Ecol 141:99–106. https://doi.org/10.1023/A:1009823015170
An H, Li GQ (2015) Effects of grazing on carbon and nitrogen in plants and soils in a semiarid desert grassland, China. J Arid Land 7:341–349. https://doi.org/10.1007/s40333-014-0049-x
Bai WM, Sun XQ, Wang ZW, Li LH (2009) Nitrogen addition and rhizome severing modify clonal growth and reproductive modes of Leymus chinensis population. Plant Ecol 205:13–21. https://doi.org/10.1007/s11258-009-9595-2
Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892. https://doi.org/10.1086/284531
Boudiar R, Casas AM, Gioia T, Fiorani F, Nagel KA, Igartua E (2020) Effects of low water availability on root placement and shoot development in landraces and modern barley cultivars. Agron J 10:134. https://doi.org/10.3390/agronomy10010134
Diabate B, Gao YZ, Li YH, Wang C, Sun BR, Folkard A, Zhou DW (2015) Associations between species distribution patterns and soil salinity in the Songnen grassland. Arid Land Res Manag 29:199–209. https://doi.org/10.1080/15324982.2014.945625
Dong M (1996) Clonal growth in plants in relation to resource heterogeneity: foraging behavior. Acta Bot Sin 38:828–835
Florence B, Guillaume T, Serge A, Jean-Yves P, Philippe C, Salvador N (2009) 13C and 15N allocations of two alpine species from early and late snowmelt locations reflect their different growth strategies. J Exp Bot 60:2725–2735. https://doi.org/10.1093/jxb/erp128
Gao Y, Wang DL, Ba L, Bai YG, Liu B (2008a) Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis. Environ Exp Bot 63:113–122. https://doi.org/10.1016/j.envexpbot.2007.10.030
Gao YZ, Giese M, Lin S, Taube F, Brueck H (2008b) Belowground net primary productivity and biomass allocation of a grassland in Inner Mongolia as affected by grazing intensity. Plant Soil 307:41–50. https://doi.org/10.1007/s11104-008-9579-3
Gao Y, Wang DL, Xing F (2014) Combined effects of resource heterogeneity and simulated herbivory on plasticity of clonal integration in a rhizomatous perennial herb. Plant Biol 16:774–782. https://doi.org/10.1111/plb.12122
Ge Y, Li JD (1990) A preliminary study on the effects of halophytes on salt accumulation and desalination in the soils of Songnen Plain, Northeast China. Acta Pratac Sin 1:70–76
Gómez S, Ferrieri RA, Schueller M, Orians CM (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188:835–844. https://doi.org/10.1111/j.1469-8137.2010.03414.x
Green RA, Detling JK (2000) Defoliation-induced enhancement of total aboveground nitrogen yield of grasses. Oikos 91:280–284. https://doi.org/10.1034/j.1600-0706.2000.910208.x
Guo JR, Zheng CC, Li YD, Fan H, Wang BS (2017) Effects of NaCl treatment on root system characteristics and activity of the euhalophyte Suaeda salsa. J Plant Physiol 53:63–70. https://doi.org/10.13592/j.cnki.ppj.2016.0521
Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565. https://doi.org/10.1111/j.1365-3040.2009.02056.x
Huhta AP, Lennartsson T, Tuomi J, Rautio P, Laine K (2000) Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol Ecol 14:373–392. https://doi.org/10.1023/A:1011028722860
Ilmarinen K, Mikola J, Vestberg M (2008) Do interactions with soil organisms mediate grass responses to defoliation? Soil Biol Biochem 40:894–905. https://doi.org/10.1016/j.soilbio.2007.11.004
Kovács L, Mendel Á, Szentgyörgyi A, Fekete S, Söre F, Posta K, Kiss E (2020) Comparative analysis of overexpressed Fragaria vesca S-adenosyl-l-methionine synthase (FvSAMS) and decarboxylase (FvSAMDC) during salt stress in transgenic Nicotiana benthamiana. Plant Growth Regul 91:53–73. https://doi.org/10.1007/s10725-020-00587-3
Landi S, Hausman J-F, Guerriero G, Esposito S (2017) Poaceae vs abiotic stress: focus on drought and salt stress, recent insights and perspectives. Front Plant Sci 8:1214. https://doi.org/10.3389/fpls.2017.01214
Li R, Shi F, Fukuda K (2010) Interactive effects of various salt and alkali stresses on growth, organic solutes, and cation accumulation in a halophyte Spartina alterniflora (Poaceae). Environ Exp Bot 68:66–74. https://doi.org/10.1016/j.envexpbot.2009.10.004
Liu Y, Wang DL, Han SJ, Cheng ZR, Du J, Wang X (2003) Variations of water-soluble carbohydrate and nitrogen contents in Leymus chinensis and Phragmites communis under different stocking rates. Chin J Appl Ecol 14:2167–2170. https://doi.org/10.13287/j.1001-9332.2003.0478
Liu JS, Wang L, Wang DL, Bonser SP, Sun F, Zhou YF, Gao Y, Teng X (2012) Plants can benefit from herbivory: stimulatory effects of sheep saliva on growth of Leymus chinensis. PLoS ONE 7:e29259. https://doi.org/10.1371/journal.pone.0029259
Liu BS, Kang CL, Wang X, Bao GZ (2015) Tolerance mechanisms of Leymus chinensis to salt-alkaline stress. Acta Agr Scand 65:723–734. https://doi.org/10.1080/09064710.2015.1054867
Liu XH, Cai SG, Wang G, Wang FF, Dong FB, Mark M, Holford P, Ji J, Salih A, Zhou MX, Shabala S, Chen ZH (2017) Halophytic NHXs confer salt tolerance by altering cytosolic and vacuolar K+ and Na+ in Arabidopsis root cell. Plant Growth Regul 82(2):333–351. https://doi.org/10.1007/s10725-017-0262-7
Luo J, Zhou JJ, Masclaux DC, Wang N, Wang H, Zheng B (2019) Morphological and physiological responses to contrasting nitrogen regimes in Populus cathayana is linked to resources allocation and carbon nitrogen partition. Environ Exp Bot 162:247–255. https://doi.org/10.1016/j.envexpbot.2019.03.003
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Newingham BA, Callaway RM, Bassirirad H (2007) Allocating nitrogen away from a herbivore: a novel compensatory response to root herbivory. Oecologia 153:913–920. https://doi.org/10.1007/s00442-007-0791-2
Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9. https://doi.org/10.1007/s00442-011-1968-2
Polley HW, Detling JK (1989) Defoliation, nitrogen, and competition: effects on plant growth and nitrogen nutrition. Ecology 70:721–727. https://doi.org/10.2307/1940222
Renninger HJ, Carlo N, Clark KL, Schafer KVR (2014) Physiological strategies of co-occurring oaks in a water- and nutrient-limited ecosystem. Tree Physiol 34:159–173. https://doi.org/10.1093/treephys/tpt122
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004
Ruess RW (1988) The interaction of defoliation and nutrient uptake in Sporobolus kentrophyllus, a short-grass species from the serengeti plains. Oecologia 77:550–556. https://doi.org/10.2307/4218818
Schmitt A, Pausch J, Kuzyakov Y (2013) C and N allocation in soil under ryegrass and alfalfa estimated by 13C and 15N labelling. Plant Soil 368:581–590. https://doi.org/10.1007/s11104-012-1536-5
Shi DC, Wang DL (2005) Effects of various saline-alkaline mixed stresses on Aneurolepidium chinense (Trin.) Kitag. Plant Soil 271:15–26. https://doi.org/10.1007/s11104-004-1307-z
Sui Y, He WM, Pan X, Dong M (2011) Partial mechanical stimulation facilitates the growth of the rhizomatous plant Leymus secalinus: modulation by clonal integration. Ann Bot 107:693–697. https://doi.org/10.1093/aob/mcr012
Sun J, Zhan TY, Liu M, Zhang ZC, Wang Y, Liu SL, Wu GL, Liu GH, Tsunekawa A (2019) Verification of the biomass transfer hypothesis under moderate grazing across the Tibetan plateau: a meta-analysis. Plant soil. https://doi.org/10.1007/s11104-019-04380-8
Tao L, Hunter MD (2013) Allocation of resources away from sites of herbivory under simultaneous attack by aboveground and belowground herbivores in the common milkweed, Asclepias syriaca. Arthropod Plant Interact 7:217–224. https://doi.org/10.1007/s11829-012-9235-y
Tuomi J, Nilsson P, Astrom M (1994) Plant compensatory responses: bud dormancy as an adaptation to herbivory. Ecology 75:1429–1436. https://doi.org/10.2307/1937466
Unkovich MJ, Sanford P, Pate J, Hyder M (1997) Effects of grazing on plant and soil nitrogen relations of pasture-crop rotations. Aust J Agr Res 49:475–485. https://doi.org/10.1071/A97071
Wang SP, Wang YF (2001) Study on over-compensation growth of Cleistogenes squarrosa population in Inner Mongolia steppe. Acta Bot Sin 43:413–418. https://doi.org/10.1093/emboj/20.7.1807
Wang ZM, Song KS, Zhang B, Liu DW, Ren CY, Luo L, Yang T, Huang N, Hu LJ, Yang HJ, Liu ZM (2009) Shrinkage and fragmentation of grasslands in the west Songnen Plain, China. Agr Ecosyst Environ 129:315–324. https://doi.org/10.1016/j.agee.2008.10.009
Ward D (2010) The effects of apical meristem damage on growth and defences of two Acacia species in the Negev Desert. Evol Ecol Res 12:589–602
Yang C, Shi D, Wang D (2008a) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regul 56:179–190. https://doi.org/10.1007/s10725-008-9299-y
Yang CW, Wang P, Li CY, Shi DC, Wang DL (2008b) Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. Photosynthetica 46:107–114. https://doi.org/10.1007/s11099-008-0018-8
Zhang W, Yang G, Sun J, Chen JS, Zhang YJ (2015) Clonal integration enhances the performance of a clonal plant species under soil alkalinity stress. PLoS ONE 10:e0119942. https://doi.org/10.1371/journal.pone.0119942
Zhao W, Chen SP, Lin GH (2008) Compensatory growth responses to clipping defoliation in Leymus chinensis (Poaceae) under nutrient addition and water deficiency conditions. Plant Ecol 196:85–99. https://doi.org/10.2307/40305476
Zheng CC, Wang YJ, Sun H, Wang XY, Gao YZ (2017) Effects of clipping on nitrogen allocation strategy and compensatory growth of Leymus chinensis under saline-alkali conditions. Chin J Appl Ecol 28:2222–2230. https://doi.org/10.13287/j.1001-9332.201707.040
Zheng CC, Ma HM, Gao YZ, Sun H, Yang HJ, Baskin CC (2019) The clonal grass Leymus chinensis overcomes salt stress by over-compensatory growth of individual ramets. Crop Pasture Sci 70:1004–1014. https://doi.org/10.1071/CP18530
Zhou C, Zhang Z, Wang ZW, Yang YF (2014) Difference in capacity of physiological integration between two ecotypes of Leymus chinensis, underlies their different performance. Plant Soil 383:191–202. https://doi.org/10.1007/s11104-014-2169-7
Zhu TC (2004) Leymus chinensis biological ecology. Jilin Science & Technology Press, Changchun
Zhu YF, Jia XM, Wu YX, Hu Y, Cheng L, Zhao T, Huang ZC, Wang YX (2020) Quantitative proteomic analysis of Malus halliana exposed to salt-alkali mixed stress reveals alterations in energy metabolism and stress regulation. Plant Growth Regul 90:205–222. https://doi.org/10.1007/s10725-019-00563-6
Zou Q (2000) The guidance of plant physiology experiment. China Agricultural Press, Beijing
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31870436, 31670446, 31471945 and U1803110), the National Key Basic Research Program of China (Grant No. 2016YFC0500703), and Jilin Special Program for Key Science and Technology Research (Grant No. Y8D1161001).
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Ma, H., Zheng, C., Gao, Y. et al. Moderate clipping stimulates over-compensatory growth of Leymus chinensis under saline-alkali stress through high allocation of biomass and nitrogen to shoots. Plant Growth Regul 92, 95–106 (2020). https://doi.org/10.1007/s10725-020-00622-3
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DOI: https://doi.org/10.1007/s10725-020-00622-3