|Breeding against mycorrhizal symbiosis: Modern cotton (Gossypium hirsutum L.) varieties perform more poorly than older varieties except at very high phosphorus supply levels
WANG Xin-xin1, 2, ZHANG Min3, SHENG Jian-dong3, FENG Gu1#, Thomas W. KUYPER4
1 College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, P.R.China
2 State Key Laboratory of North China Crop Improvement and Regulation/Mountain Area Research Institute, Hebei Agricultural University, Baoding 071001, P.R.China
3 College of Resource and Environmental Sciences, Xinjiang Agricultural University, Urumqi 830052, P.R.China
4 Soil Biology Group, Wageningen University & Research, Wageningen 6700AA, The Netherlands
棉花（Gossypium hirsutum L.）是一种重要的纤维经济作物，以往对于棉花获取磷（P）相关的根系性状（包括菌根根系性状）的研究较少。我们采用1950年至2013年在中国西北地区使用的8个棉花品种在3种磷供应水平下（分别为0、50和300 mg KH2PO4 kg-1），研究了接种或者不接种丛枝菌根真菌Funneliformis mosseae棉花的生长和11个根系性状特征。结果表明：与老品种相比，新品种的根系直径更细，地上部吸收的磷更少，苗期生物量更低。这表明育种过程选择了更细的根系，菌根真菌定殖的皮层空间更少，因而增加了对供磷强度的更高需求。在两个低磷水平下，菌根植物比非菌根植物吸收更多的磷，产生更多的生物量（在P0时，3.2 mg对0.9 mg，1.8 g对0.9 g；在P50时，14.5 mg对1.7 mg， 4.7 g对1.6 g）。在最高磷水平下，菌根植物比非菌根植物获得更多的磷（18.8 mg对13.4 mg ），但生物量没有差异（6.2 g对6.3 g）。在中等供磷（P50）水平下，根系直径与菌根植物地上部生物量、磷浓度和磷含量呈显著正相关。我们的结果支持了植物获取磷的外包模式（即借助菌根途径）在根系经济学空间框架中的重要性。在过去的几十年里，育种使得棉花的根系更细、从菌根途径获益更低，这导致了在中等磷供应并有菌根侵染条件下，老品种的生物量显著大于新品种的生物量。未来棉花品种选育的策略要考虑到在根系自身吸收磷的能力和发挥菌根吸磷能力之间的权衡（即根系性状与菌根性状的权衡），以便选育出在中等磷肥投入条件下实现高产的品种。
Cotton (Gossypium hirsutum L.) is an important fiber cash crop, but its root traits related to phosphorus (P) acquisition, including mycorrhizal root traits, are poorly understood. Eight cotton varieties bred in northwestern China that were released between 1950 and 2013 were grown in pots with or without one arbuscular mycorrhizal fungal (AMF) species (Funneliformis mosseae) at three P supply levels (0, 50 and 300 mg P as KH2PO4 kg–1). Eleven root traits were measured and calculated after 7 wk of growth. The more recent accessions had smaller root diameters, acquired less P and produced less biomass, indicating an (inadvertent) varietal selection for thinner roots that provided less cortical space for AMF, which then increased the need for a high P fertilizer level. At the two lower P levels, the mycorrhizal plants acquired more P and produced more biomass than non-mycorrhizal plants (3.2 vs. 0.9 mg P per plant; 1.8 vs. 0.9 g biomass per plant at P0; 14.5 vs. 1.7 mg P per plant; and 4.7 vs. 1.6 g biomass per plant at P50). At the highest P level, the mycorrhizal plants acquired more P than non-mycorrhizal plants (18.8 vs. 13.4 mg per P plant), but there was no difference in biomass (6.2 vs. 6.3 g per plant). At the intermediate P level, root diameter was significantly positively correlated with shoot biomass, P concentration and the P content of mycorrhizal plants. The results of our study support the importance of the outsourcing model of P acquisition in the root economics space framework. Inadvertent varietal selection in the last decades, resulting in thinner roots and a lower benefit from AMF, has led to a lower productivity of cotton varieties at moderate P supply (i.e., when mycorrhizal, the average biomass of older varieties 5.0 g per plant vs. biomass of newer varieties 4.4 g per plant), indicating the need to rethink cotton breeding efforts in order to achieve high yields without very high P input. One feasible way to solve the problem of inadvertent varietal selection for cotton is to be aware of the trade-offs between the root do-it-yourself strategy and the outsourcing towards AMF strategy, and to consider both morphological and mycorrhizal root traits when breeding cotton varieties.
Received: 27 September 2021
Accepted: 10 November 2021
This study was financially supported by the National Natural Science Foundation of China (32272807 and U1703232). Wang Xinxin is supported via project from State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2021ZZ-1).
|About author: #Correspondence FENG Gu, Tel: +86-10-62733885, Fax: +86-10-62731016, E-mail: email@example.com
Cite this article:
WANG Xin-xin, ZHANG Min, SHENG Jian-dong, FENG Gu, Thomas W. KUYPER.
Breeding against mycorrhizal symbiosis: Modern cotton (Gossypium hirsutum L.) varieties perform more poorly than older varieties except at very high phosphorus supply levels. Journal of Integrative Agriculture, 22(3): 701-715.
| Alvey S, Bagayoko M, Neumann G, Buerkert A. 2001. Cereal/legume rotations affect chemical properties and biological activities in two West African soils. Plant and Soil, 231, 45–54.
An G H, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, Ezawa T. 2010. How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant and Soil, 327, 441–453.
Bardgett R D, Mommer L, De Vries F T. 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology and Evolution, 29, 692–699.
Bergmann J, Weigelt A, van Der Plas F, Laughlin D C, Kuyper T W, Guerrero-Ramirez N R, Valverde-Barrantes O J, Bruelheide H, Freschet G T, Iversen C M, Kattge J, Mccormack M L, Meier I C, Rillig M C, Roumet C, Semchenko M, Sweeney C J, van Ruijven J, York L M, Mommer L. 2020. The fungal collaboration gradient dominates the root economics space in plants. Science Advances, 6, eaba3756.
Blaas H, Kroeze C. 2016. Excessive nitrogen and phosphorus in European rivers: 2000–2050. Ecological Indicators, 67, 328–337.
Cely M V T, de Oliveira A G, de Freitas V F, de Luca M B, Barazetti A R, dos Santos I M O, Gionco B, Garcia G V, Prete C E C, Andrade G. 2016. Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Frontiers in Microbiology, 7, 720.
Chen B L, Wang Q H, Bucking H, Sheng J D, Luo J, Chai Z P, Kafle A, Hou Y Y, Feng G. 2019. Genotypic differences in phosphorus acquisition efficiency and root performance of cotton (Gossypium hirsutum) under low-phosphorus stress. Crop and Pasture Science, 70, 344–358.
Damodaran P N, Udaiyan K, Roh K S. 2012. Mycorrhizal dependency in certain Indian cotton cultivars. Research in Plant Biology, 2, 55–66.
Eskandari S, Guppy C N, Knox O G G, Backhouse D, Haling R E. 2018. Understanding the impact of soil sodicity on mycorrhizal symbiosis: some facts and gaps identified from cotton systems. Appllied Soil Ecology, 126, 199–201.
Eskandari S, Guppy C N, Knox O G G, Flavel R J, Backhouse D, Haling R E. 2017. Mycorrhizal contribution to phosphorus nutrition of cotton in low and highly sodic soils using dual isotope labelling (32P and 33P). Soil Biology and Biochemistry, 105, 37–44.
Fageria N K. 2014. Growth, nutrient uptake, and use efficiency in dry bean in tropical upland soil. Journal of Plant Nutrition, 37, 2085–2093.
Fageria N K, Gheyi H R, Carvalho M C S, Moreira A. 2016. Root growth, nutrient uptake and use efficiency by roots of tropical legume cover crops as influenced by phosphorus fertilization. Journal of Plant Nutrition, 39, 781–792.
Feng L, Chi B J, Dong H Z. 2022. Cotton cultivation technology with Chinese characteristics has driven the 70-year development of cotton production in China. Journal of Integrative Agriculture, 21, 597–609.
Galván G A, Kuyper T W, Burger K, Keizer L C P, Hoekstra R F, Kik C, Scholten O E. 2011. Genetic analysis of the interaction between Allium species and arbuscular mycorrhizal fungi. Theoretical and Applied Genetics, 122, 947–960.
Gill M A, Sabir M, Ashraf S, Rahmatullah, Aziz T. 2005. Effect of P-stress on growth, phosphorus uptake and utilization efficiency of different cotton cultivars. Pakistan Journal of Agricultural Sciences, 42, 42–47.
Jakobsen I, Abbott L K, Robson A D. 1992. External hyphae of vesicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytologist, 120, 509–516.
Janos D P. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza, 17, 75–91.
Kaeppler S M, Parke J L, Mueller S M, Senior L, Stuber C, Tracy W F. 2000. Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Science, 40, 358–364.
Kuyper T W, Wang X X, Muchane M N. 2021. The interplay between roots and arbuscular mycorrhizal fungi influencing water and nutrient acquisition and use efficiency. In: Rengel Z, Djalovic I, eds., The Root Systems in Sustainable Agricultural Intensification. John Wiley & Sons Inc., New Jersey, USA.
Lambers H, Shane M W, Cramer M D, Pearse S J, Veneklaas E J. 2006. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany, 98, 693–713.
Lehmann A, Barto E K, Powell J R, Rillig M C. 2012. Mycorrhizal responsiveness trends in annual crop plants and their wild relatives - A meta analysis on studies from 1981 to 2010. Plant and Soil, 355, 231–250.
Lekberg Y, Koide R T. 2005. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytologist, 168, 189–204.
Li H, Ma Q, Li H, Zhang F S, Rengel Z, Shen J B. 2014. Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits. Plant and Soil, 376, 151–163.
Liu S L, Guo X L, Feng G, Maimaitiaili B, Fan J L, He X H. 2016. Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant and Soil, 398, 195–206.
Liu Y, Villalba G, Ayres R U, Schroder H. 2008. Global phosphorus flows and environmental impacts from a consumption perspective. Journal of Industrial Ecology, 12, 229–247.
Lynch J P. 2019. Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytologist, 223, 548–564.
Mai W, Xue X, Feng G, Yang R, Tian C. 2018. Can optimization of phosphorus input lead to high productivity and high phosphorus use efficiency of cotton through maximization of root/mycorrhizal efficiency in phosphorus acquisition? Field Crops Research, 216, 100–108.
Martin-Robles N, Morente-Lopez J, Freschet G T, Poorter H, Roumet C, Milla R. 2019. Root traits of herbaceous crops: pre-adaptation to cultivation or evolution under domestication? Functional Ecology, 33, 273–285.
McGonigle T, Miller M, Evans D, Fairchild G, Swan J. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist, 115, 495–501.
McMichael B L, Burke J J, Berlin J D, Hatfield J L, Quisenberry J E. 1985. Root vascular bundle arrangements among cotton strains and cultivars. Environmental and Experimental Botany, 25, 23–30.
Murphy J, Riley J P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36.
Nehl D B, McGee P A. 2010. Ecophysiology of arbuscular mycorrhizas in cotton. In: Stewart J M, Oosterhuis D M, Heitholt J J, Mauney J R, eds., Physiology of Cotton. Springer Netherlands, Dordrecht. pp. 206–212.
Neumann G. 2006. Quantitative determination of acid phosphatase activity in the rhizosphere and on the root surface. In: Luster J, Finlay R, eds., Handbook of Methods used in Rhizosphere Research. pp. 418–442.
Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker M, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn A, Pronk A. 2007. Specific root length as an indicator of environmental change. Plant Biosystems, 141, 426–442.
Pang J, Yang J, Lambers H, Tibbett M, Siddique K H M, Ryan M H. 2015. Physiological and morphological adaptations of herbaceous perennial legumes allow differential access to sources of varyingly soluble phosphate. Physiologia Plantarum, 154, 511–525.
Raghothama K G. 1999. Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 665–693.
Reich P B. 2014. The world-wide ‘fast-slow’ plant economics spectrum: A traits manifesto. Journal of Ecology, 102, 275–301.
Salgado F H M, Moreira F M D, Siqueira J O, Barbosa R H, Paulino H B, Carneiro M A C. 2017. Arbuscular mycorrhizal fungi and colonization stimulant in cotton and maize. Ciencia Rural, 47, e20151535.
Sawers R J H, Gebreselassie M N, Janos D P, Paszkowski U. 2010. Characterizing variation in mycorrhiza effect among diverse plant varieties. Theoretical and Applied Genetics, 120, 1029–1039.
Seifert E K, Bever J D, Maron J L. 2009. Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology, 90, 1055–1062.
Singh V, Pallaghy C K, Singh D. 2006. Phosphorus nutrition and tolerance of cotton to water stress: I. Seed cotton yield and leaf morphology. Field Crops Research, 96, 191–198.
Valverde-Barrantes O J, Horning A L, Smemo K A, Blackwood C B. 2016. Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant and Soil, 404, 1–12.
Vance C P, Uhde-Stone C, Allan D L. 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist, 157, 423–447.
Veneklaas E J, Stevens J, Cawthray G R, Turner S, Grigg A M, Lambers H. 2003. Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant and Soil, 248, 187–197.
Wang L T, Wang X H, Maimaitiaili B, Kafle A, Khan K S, Feng G. 2021. Breeding practice improves the mycorrhizal responsiveness of cotton (Gossypium spp. L.). Frontiers in Plant Science, 12, 780454.
Wang X J, Tang C X, Guppy C N, Sale P W G. 2010. Cotton, wheat and white lupin differ in phosphorus acquisition from sparingly soluble sources. Environmental and Experimental Botany, 69, 267–272.
Wang X X, Li H B, Chu Q, Feng G, Kuyper T W, Rengel Z. 2020a. Mycorrhizal impacts on root trait plasticity of six maize varieties along a phosphorus supply gradient. Plant and Soil, 448, 71–86.
Wang X X, van der Werf W, Yu Y, Hoffland E, Feng G, Kuyper T W. 2020b. Field performance of different maize varieties in growth cores at natural and reduced mycorrhizal colonization: yield gains and possible fertilizer savings in relation to phosphorus application. Plant and Soil, 450, 613–624.
Xiao S, Liu L T, Zhang Y J, Sun H C, Zhang K, Bai Z Y, Dong H Z, Li C D. 2020. Fine root and root hair morphology of cotton under drought stress revealed with RhizoPot. Journal of Agronomy and Crop Science, 206, 679–693.
Yan Z, Liu P, Li Y, Ma L, Alva A, Dou Z, Chen Q, Zhang F. 2013. Phosphorus in China’s intensive vegetable production systems: Overfertilization, soil enrichment, and environmental implications. Journal of Environmental Quality, 42, 982–989.
Zak J C, McMichael B, Dhillion S, Friese C. 1998. Arbuscular-mycorrhizal colonization dynamics of cotton (Gossypium hirsutum L.) growing under several production systems on the Southern High Plains, Texas. Agriculture Ecosystems and Environment, 68, 245–254.
Zhang W F, Ma W Q, Ji Y X, Fan M S, Oenema O, Zhang F S. 2008. Efficiency, economics, and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutrient Cycling in Agroecosystems, 80, 131–144.
Zhang W W, Wang C, Xue R, Wang L J. 2019. Effects of salinity on the soil microbial community and soil fertility. Journal of Integrative Agriculture, 18, 1360–1368.
Zhu J M, Lynch J P. 2004. The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Functional Plant Biology, 31, 949–958.
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