|
|
Improving the efficiency and effectiveness of global phosphorus use: focus on root and rhizosphere levels in the agronomic system |
Uwe LUDEWIG1(), Lixing YUAN2, Günter NEUMANN1 |
1. Crop Science Institute, Nutritional Crop Physiology (340h), University of Hohenheim, Fruwirthstr. 20, D-70593 Stuttgart, Germany 2. National Academy of Agriculture Green Development, Key Laboratory of Plant-Soil Interactions (Ministry of Education), College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China |
|
|
Abstract Phosphorus (P) is essential for life and for efficient crop production, but global P use with limited recycling is inefficient in several sectors, including agronomy. Unfortunately, plant physiologists, agronomists, farmers and end users employ different measures for P use efficiency (PUE), which often masks their values at different scales. The term P use effectiveness, which also considers energetic and sustainability measures in addition to P balances, is also a valuable concept. Major physiological and genetic factors for plant P uptake and utilization have been identified, but there has been limited success in genetically improving PUE of modern crop cultivars. In maize, studies on root architectural and morphological traits appear promising. Rhizosphere processes assist in mobilizing and capturing sparingly soluble phosphate from rock phosphate. Combinations of phosphate-solubilizing microorganisms with ammonium-based nitrogen fertilizer, as well as strategies of fertilizer placement near the roots of target crops, can moderately enhance PUE. The desired concentration of P in the products differs, depending on the final use of the crop products as feed, food or for energy conversion, which should be considered during crop production.
|
Keywords
acquisition efficiency
plant growth promoting rhizobacteria
phosphate
use efficiency
utilization efficiency
|
Corresponding Author(s):
Uwe LUDEWIG
|
Just Accepted Date: 01 August 2019
Online First Date: 25 September 2019
Issue Date: 29 November 2019
|
|
1 |
P Marschner. Marschner’s mineral nutrition of higher plants. London: Academic Press, 2011
|
2 |
D L Jones, P G Dennis, A G Owen, P A W van Hees. Organic acid behaviour in soils: misconceptions and knowledge gaps. Plant and Soil, 2003, 248(1–2): 31–41
https://doi.org/10.1023/A:1022304332313
|
3 |
M Hens, B L Turner, P J Hocking. Chemical nature of soil organic phosphorus mobilized by organic anions. In: Proceedings of the 2nd International Symposium on Phosphorus Dynamics in the Soil-Plant Continuum 2005, Perth. Dordrecht, the Netherlands: Kluwer Academic Publishers, 2005, 16–17
|
4 |
G Neumann, V Römheld. The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri Z, eds. The rhizosphere: biochemistry and organic substances at the soil-plant interface. 2nd ed. Boca Raton: CRC Press, 2007, 23–72
|
5 |
A E Richardson, T S George, M Hens, R J Simpson. Utilization of soil organic phosphorus by higher plants. In: Turner B L, Frossard E, Baldwin D, eds. Organic phosphorus in the environment. Cambridge, MA, USA: CAB International, 2005, 165–184
|
6 |
U Irshad, A Brauman, C Villenave, C Plassard. Phosphorus acquisition from phytate depends on efficient bacterial grazing, irrespective of the mycorrhizal status of Pinus pinaster. Plant and Soil, 2012, 358(1–2): 155–168
https://doi.org/10.1007/s11104-012-1161-3
|
7 |
D P Schachtman, R J Reid, S M Ayling. Phosphorus uptake by plants: from soil to cell. Plant Physiology, 1998, 116(2): 447–453
https://doi.org/10.1104/pp.116.2.447
pmid: 9490752
|
8 |
D Cordell, T S Neset, T Prior. The phosphorus mass balance: identifying ‘hotspots’ in the food system as a roadmap to phosphorus security. Current Opinion in Biotechnology, 2012, 23(6): 839–845
https://doi.org/10.1016/j.copbio.2012.03.010
pmid: 22503084
|
9 |
D Cordell, A Rosemarin, J J Schröder, A L Smit. Towards global phosphorus security: a systems framework for phosphorus recovery and reuse options. Chemosphere, 2011, 84(6): 747–758
https://doi.org/10.1016/j.chemosphere.2011.02.032
pmid: 21414650
|
10 |
H Lambers, J C Clements, M N Nelson. How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). American Journal of Botany, 2013, 100(2): 263–288
https://doi.org/10.3732/ajb.1200474
pmid: 23347972
|
11 |
J Liu, L Yang, M Luan, Y Wang, C Zhang, B Zhang, J Shi, F G Zhao, W Lan, S Luan. A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(47): E6571–E6578
https://doi.org/10.1073/pnas.1514598112
pmid: 26554016
|
12 |
Y S Rahayu, P Walch-Liu, G Neumann, V Römheld, N von Wirén, F Bangerth. Root-derived cytokinins as long-distance signals for NO3–-induced stimulation of leaf growth. Journal of Experimental Botany, 2005, 56(414): 1143–1152
https://doi.org/10.1093/jxb/eri107
pmid: 15710629
|
13 |
R Wild, R Gerasimaite, J Y Jung, V Truffault, I Pavlovic, A Schmidt, A Saiardi, H J Jessen, Y Poirier, M Hothorn, A Mayer. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science, 2016, 352(6288): 986–990
https://doi.org/10.1126/science.aad9858
pmid: 27080106
|
14 |
R H Moll, E J Kamprath, W A Jackson. Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal, 1982, 74(3): 562–564
https://doi.org/10.2134/agronj1982.00021962007400030037x
|
15 |
A G Good, A K Shrawat, D G Muench. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science, 2004, 9(12): 597–605
https://doi.org/10.1016/j.tplants.2004.10.008
pmid: 15564127
|
16 |
L K Brown, T S George, J A Thompson, G Wright, J Lyon, L Dupuy, S F Hubbard, P J White. What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Annals of Botany, 2012, 110(2): 319–328
https://doi.org/10.1093/aob/mcs085
pmid: 22539540
|
17 |
F Klamer, F Vogel, X Li, H Bremer, G Neumann, B Neuhauser, F Hochholdinger, U Ludewig. Estimating the importance of maize root hairs in low phosphorus conditions and under drought. Annals of Botany, 2019 [Published Online]. doi: 10.1093/aob/mcz011
|
18 |
F Wang, T Rose, K Jeong, T Kretzschmar, M Wissuwa. The knowns and unknowns of phosphorus loading into grains, and implications for phosphorus efficiency in cropping systems. Journal of Experimental Botany, 2016, 67(5): 1221–1229
https://doi.org/10.1093/jxb/erv517
pmid: 26662950
|
19 |
V Raboy. Approaches and challenges to engineering seed phytate and total phosphorus. Plant Science, 2009, 177(4): 281–296
https://doi.org/10.1016/j.plantsci.2009.06.012
|
20 |
E Doria, L Galleschi, L Calucci, C Pinzino, R Pilu, E Cassani, E Nielsen. Phytic acid prevents oxidative stress in seeds: evidence from a maize (Zea mays L.) low phytic acid mutant. Journal of Experimental Botany, 2009, 60(3): 967–978
https://doi.org/10.1093/jxb/ern345
pmid: 19204030
|
21 |
Z Li, X Zhang, Y Zhao, Y Li, G Zhang, Z Peng, J Zhang. Enhancing auxin accumulation in maize root tips improves root growth and dwarfs plant height. Plant Biotechnology Journal, 2018, 16(1): 86–99
https://doi.org/10.1111/pbi.12751
pmid: 28499064
|
22 |
S Wang, S Zhang, C Sun, Y Xu, Y Chen, C Yu, Q Qian, D A Jiang, Y Qi. Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytologist, 2014, 201(1): 91–103
https://doi.org/10.1111/nph.12499
pmid: 24111723
|
23 |
Y Lyu, H Tang, H Li, F Zhang, Z Rengel, W R Whalley, J Shen. Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply. Frontiers of Plant Science, 2016, 7: 1939
https://doi.org/10.3389/fpls.2016.01939
pmid: 28066491
|
24 |
D Föhse, N Claassen, A Jungk. Phosphorus efficiency of plants. II. Significance of root hairs and cation-anion balance for phosphorus influx in seven plant species. Plant and Soil, 1991, 132(2): 261–272
https://doi.org/10.1007/BF00010407
|
25 |
Z Wen, H Li, Q Shen, X Tang, C Xiong, H Li, J Pang, M H Ryan, H Lambers, J Shen. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytology, 2019 [Published Online]. doi: 10.1111/nph.15833
|
26 |
G Neumann, T S George, C Plassard. Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant and Soil, 2009, 321(1–2): 431–456
https://doi.org/10.1007/s11104-009-9953-9
|
27 |
J Nestler, S D Keyes, M Wissuwa. Root hair formation in rice (Oryza sativa L.) differs between root types and is altered in artificial growth conditions. Journal of Experimental Botany, 2016, 67(12): 3699–3708
https://doi.org/10.1093/jxb/erw115
pmid: 26976815
|
28 |
J P Lynch. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology, 2011, 156(3): 1041–1049
https://doi.org/10.1104/pp.111.175414
pmid: 21610180
|
29 |
R Gamuyao, J H Chin, J Pariasca-Tanaka, P Pesaresi, S Catausan, C Dalid, I Slamet-Loedin, E M Tecson-Mendoza, M Wissuwa, S Heuer. The protein kinase PSTOL1 from traditional rice confers tolerance of phosphorus deficiency. Nature, 2012, 488(7412): 535–539
https://doi.org/10.1038/nature11346
pmid: 22914168
|
30 |
G C Azevedo, A Cheavegatti-Gianotto, B F Negri, B Hufnagel, L C e Silva, J V Magalhaes, A A Garcia, U G Lana, S M de Sousa, C T Guimaraes. Multiple interval QTL mapping and searching for PSTOL1 homologs associated with root morphology, biomass accumulation and phosphorus content in maize seedlings under low-P. BMC Plant Biology, 2015, 15(1): 172
https://doi.org/10.1186/s12870-015-0561-y
pmid: 26148492
|
31 |
Z Liu, X Liu, E J Craft, L Yuan, L Cheng, G Mi, F Chen. Physiological and genetic analysis for maize root characters and yield in response to low phosphorus stress. Breeding Science, 2018, 68(2): 268–277
https://doi.org/10.1270/jsbbs.17083
pmid: 29875611
|
32 |
Z Liu, K Gao, S Shan, R Gu, Z Wang, E J Craft, G Mi, L Yuan, F Chen. Comparative analysis of root traits and the associated QTLs for maize seedlings grown in paper roll, hydroponics and vermiculite culture system. Frontiers of Plant Science, 2017, 8: 436
https://doi.org/10.3389/fpls.2017.00436
pmid: 28424719
|
33 |
R Gu, F Chen, L Long, H Cai, Z Liu, J Yang, L Wang, H Li, J Li, W Liu, G Mi, F Zhang, L Yuan. Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize. Journal of Genetics and Genomics, 2016, 43(11): 663–672
https://doi.org/10.1016/j.jgg.2016.11.002
pmid: 27889500
|
34 |
R Gu, F Chen, B Liu, X Wang, J Liu, P Li, Q Pan, J Pace, A A Soomro, T Lübberstedt, G Mi, L Yuan. Comprehensive phenotypic analysis and quantitative trait locus identification for grain mineral concentration, content, and yield in maize (Zea mays L.). Theoretical and Applied Genetics, 2015, 128(9): 1777–1789
https://doi.org/10.1007/s00122-015-2546-5
pmid: 26058362
|
35 |
G Berg, K Smalla. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 2009, 68(1): 1–13
https://doi.org/10.1111/j.1574-6941.2009.00654.x
pmid: 19243436
|
36 |
E I Newman. The rhizosphere: carbon sources and microbial populations. In: Fitter A H, ed. Ecological interactions in soil. Oxford, UK: Special Publications No 4 of the British Ecological Society, Blackwell Scientific Publications, 1985: 107–121
|
37 |
R Mendes, M Kruijt, I de Bruijn, E Dekkers, M van der Voort, J H Schneider, Y M Piceno, T Z DeSantis, G L Andersen, P A Bakker, J M Raaijmakers. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 2011, 332(6033): 1097–1100
https://doi.org/10.1126/science.1203980
pmid: 21551032
|
38 |
K Zhalnina, K B Louie, Z Hao, N Mansoori, U N da Rocha, S Shi, H Cho, U Karaoz, D Loqué, B P Bowen, M K Firestone, T R Northen, E L Brodie. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nature Microbiology, 2018, 3(4): 470–480
https://doi.org/10.1038/s41564-018-0129-3
pmid: 29556109
|
39 |
S Windisch, S Bott, M A Ohler, H P Mock, R Lippmann, R Grosch, K Smalla, U Ludewig, G Neumann. Rhizoctonia solani and bacterial inoculants stimulate root exudation of antifungal compounds in lettuce in a soil-type specific manner. Agronomy, 2017, 7(2): 44
https://doi.org/10.3390/agronomy7020044
|
40 |
S Cesco, G Neumann, N Tomasi, R Pinton, L Weisskopf. Marschner review: release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil, 2010, 329(1–2): 1–25
https://doi.org/10.1007/s11104-009-0266-9
|
41 |
L Schütz, A Gattinger, M Meier, A Müller, T Boller, P Mäder, N Mathimaran. Improving crop yield and nutrient use efficiency via biofertilization—a global meta-analysis. Frontiers of Plant Science, 2018, 8: 2204
https://doi.org/10.3389/fpls.2017.02204
pmid: 29375594
|
42 |
G Neumann. Final report of Biofector project, 2017. Available at BIOFECOR website on May 20, 2019
|
43 |
K Bradáčová, A S Florea, A Bar-Tal, D Minz, U Yermiyahu, R Shawahna, J Kraut-Cohen, A Zolti, R Erel, K Dietel, M Weinmann, B Zimmermann, N Berger, U Ludewig, G Neumann, G Poşta. Microbial consortia versus single-strain inoculants: an advantage in PGPM-assisted tomato production? Agronomy, 2019, 9(2): 105
https://doi.org/10.3390/agronomy9020105
|
44 |
N Eltlbany, M Baklawa, G C Ding, D Nassal, N Weber, E Kandeler, G Neumann, U Ludewig, L S van Overbeek, K Smalla. Enhanced tomato plant growth in soil under reduced P supply through microbial inoculants and microbiome shifts. FEMS Microbiology Ecology, 2019 [in Press]. doi: 10.1093/femsec/fiz124
|
45 |
C Thonar, J D S Lekfeldt, V Cozzolino, D Kundel, M Kulhánek, C Mosimann, G Neumann, A Piccolo, M Rex, S Symanczik, F Walder, M Weinmann, A de Neergaard, P Mäder. Potential of three microbial bio-effectors to promote maize growth and nutrient acquisition from alternative phosphorous fertilizers in contrasting soils. Chemical and Biological Technologies in Agriculture, 2017, 4(1): 7
https://doi.org/10.1186/s40538-017-0088-6
|
46 |
V Römheld. pH changes in the rhizosphere of various crop plants, in relation to the supply of plant nutrients. Berne, Switzerland: Potash Review, 1986, 12(6/55): 1–8
|
47 |
J Y Jing, Y K Rui, F S Zhang, Z Rengel, J B Shen. Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification. Field Crops Research, 2010, 119(2–3): 355–364
https://doi.org/10.1016/j.fcr.2010.08.005
|
48 |
I K Mpanga, P M Nkebiwe, M Kuhlmann, V Cozzolino, A Piccolo, J Geistlinger, N Berger, U Ludewig, G Neumann. The form of N supply determines plant growth promotion by P-solubilizing microorganisms in maize. Microorganisms, 2019, 7(2): 38
https://doi.org/10.3390/microorganisms7020038
pmid: 30699936
|
49 |
I K Mpanga, H K Dapaah, J Geistlinger, U Ludewig, G Neumann. Soil type-dependent interactions of P-solubilizing microorganisms with organic and inorganic fertilizers mediate plant growth promotion in tomato. Agronomy, 2018, 8(10): 213
https://doi.org/10.3390/agronomy8100213
|
50 |
S N Pandey. Biomolecular functions of micronutrients toward abiotic stress tolerance in plants. In: Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B, eds. Plant nutrients and abiotic stress tolerance. Singapore: Springer, 2018, 153–170
|
51 |
L E Datnoff, W E Elmer, D M Huber. Mineral nutrition and plant disease. St Paul, Minnesota, USA: APS Press, 2007
|
52 |
H Huber, T S McCay-Buis. A multiple component analysis of the take-all disease of cereals. Plant Disease, 1993, 77(5): 437–447
https://doi.org/10.1094/PD-77-0437
|
53 |
L M York, T Galindo-Castañeda, J R Schussler, J P Lynch. Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. Journal of Experimental Botany, 2015, 66(8): 2347–2358
https://doi.org/10.1093/jxb/erv074
pmid: 25795737
|
54 |
D Zhang, C Zhang, X Tang, H Li, F Zhang, Z Rengel, W R Whalley, W J Davies, J Shen. Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytologist, 2016, 209(2): 823–831
https://doi.org/10.1111/nph.13613
pmid: 26313736
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|