Mapping the scientific knowledge of glomalin-related soil protein with implications for carbon sequestration

Figures & data

Figure 1. The study selection and flow chart of the research framework.

Figure 2. (a) Document type percentage of reports for GRSP research; (b) Distribution of different research directions and number of papers for GRSP per year.

Table 1. The top 11 journals for GRSP research.

Rank	Journal	N (%)	Citations	Citations/N	Country	IF (2020)
1	Soil Biology & Biochemistry	53(8.36%)	2853	53.83	England	7.609/Q1
2	Applied Soil Ecology	28(4.42%)	614	21.93	Netherlands	4.046/Q1
3	Soil Tillage Research	22(3.47%)	840	38.18	Netherlands	5.374/Q1
4	Plant and Soil	18(2.84%)	2088	116	Netherlands	4.192/Q1
5	Science of the Total Environment	16(2.52%)	508	31.75	Netherlands	7.963/Q1
6	Archives of Agronomy and Soil Science	15(2.37%)	85	5.67	England	3.092/Q2
7	Catena	15(2.37%)	134	8.93	Germany	5.198/Q1
8	Mycorrhiza	13(2.05%)	359	27.62	Germany	3.387/Q2
9	Geoderma	11(1.74%)	274	24.91	Netherlands	6.114/Q1
10	Scientific Reports	10(1.58%)	233	23.3	England	4.379/Q1
11	Soil Science Society of America Journal	10(1.42%)	622	62.2	USA	2.3068/Q3

Note: N: number; IF: Impact factor (value shows journal quality)

Figure 3. The network map of (a) the top 36 productive countries, and (b) the top 25 productive institutions for GRSP research.

Figure 4. The global distribution of authors for GRSP research.

Table 2. The top 10 cited papers in GRSP research.

Rank	Title	Author(s) (Publication year)	Orgnization (Country)	Citation	Average per Year
1	Mycorrhizas and soil structure	Rillig and Mummey (2006)	Univ Montana (USA)	756	47.25
2	A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi	Wright and Upadhyaya (1998)	USAD ARS (USA)	657	27.38
3	Arbuscular mycorrhizae, glomalin, and soil aggregation	Rillig (2004b)	Univ Montana (USA)	466	25.89
4	Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments	Wilson et al. (2009)	Oklahoma State Univ (USA)	383	29.46
5	Rote of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation	Khan (2005)	Univ Western Sydney (Australia)	346	20.35
6	Arbuscular mycorrhizae and terrestrial ecosystem processes	Rillig (2004a)	Univ Montana (USA)	346	19.22
7	Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils	Rillig, Wright, and Nichols et al. (2001b)	Univ Montana (USA)	327	15.57
8	The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species	Rillig, Wright, and Eviner (2002)	Univ Montana (USA)	292	14.6
9	The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements	Gonzalez-Chavez et al. (2004)	Nat Resources Inst, Colegio Postgrad, Mexico City	262	14.56
10	Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi	Driver, Holben, and Rillig (2005)	Univ Montana (USA)	212	12.47

Table 3. The top 10 active authors for GRSP research.

Rank	Author	N	Citations	Citations/N	Country
1	Rillig,MC	41	5079	123.88	USA
2	Wu,Qiang-Sheng	36	651	18.08	China
3	Wright,SF	28	3103	110.82	USA
4	Borie,Fernndo	25	931	37.24	Chile
5	Cornejo,Pablo	24	779	32.46	Chile
6	Zou,Ying-ning	18	660	36.67	China
7	Srivastava,A.K.	14	323	23.07	India
8	Roldan,A.	12	657	54.75	Spain
9	Nichols,Ka	10	887	88.7	USA
10	Seguel,Alex	9	243	27	Chile

Figure 5. (a) Network and (b) overlay visualization map of co-occurrence keywords for GRSP research from 1998 to 2021. The colors in (a) represent different clusters, and the colors in (b) represent the average time of keyword occurrence.

Figure 6. (a) Network and (b) overlay visualization map of co-occurrence keywords for GRSP research from 1998 to 2021.

Figure 7. Top 19 keywords with the strongest citation burst.

Table 4. Benefits of GRSP for soil and plants.

Object	The role of GRSP	Mechanisms and examples		References
Soil	improve soil structure	promote the formation of soil aggregates and improve the stability of soil aggregates	improve the physical growing space of its fungal and plant roots	Rillig et al. 2001b; Rillig and Steinberg 2002; Wright and Upadhyaya 1998
	reduce soil pollution	adsorb and stabilize heavy metals, chelate with heavy metals	have biological stability for Cu, Cd, Cr, Pb, Zn and Ar	Riaz, Kamran, and Fang et al. 2021
	Promote carbon cycle and carbon sequestration	the most important source of SOC	have abundant carbon (5–13%)	Kumar, Singh, and Ghosh 2018; Lovelock et al. 2004
		have high soil accumulation capacity	have a turnover time of 6–42 years	Rillig, et al. 2001; Gao, Wang, and Wu 2019
		reduce SOC decomposition	promote the formation of water stable aggregates to protect SOC	Agnihotri et al. 2022
	improve soil quality	an indicator of soil quality recovery		Singh, Zhu, and Chen et al. 2020
Plants	improve the tolerance of plants	improve soil water retention capacity	improve drought tolerance of plants	Rillig 2004a; Wu, Xia, and Zou 2008
		counteract the adverse effect of disturbed soil aggregation under high NaCl levels	improve salt tolerance of plants	Hammer, Rillig, and Nielsen 2011
		bind with toxic metals, stabilize them and isolate their availability	reduce the toxicity of toxic metals to plants	Vodnik et al. 2008
	promote plant growth	improve soil structure	improve the physical growing space of its fungal and plant roots; and AMF also promotes plant growth	Rillig, et al. 2001; Rillig and Steinberg 2002; Wright and Upadhyaya 1998

Rillig, M. C., and D. L. Mummey. 2006. “Mycorrhizas and Soil Structure.” The New Phytologist 171 (1): 41–53. doi:10.1111/j.1469-8137.2006.01750.x.

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Wright, S. F., and A. Upadhyaya. 1998. “A Survey of Soils for Aggregate Stability and Glomalin, A Glycoprotein Produced by Hyphae of Arbuscular Mycorrhizal Fungi.” Plant and Soil 198 (1): 97–107. doi:10.1023/a:1004347701584.

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Rillig, M. C. 2004a. “Arbuscular Mycorrhizae and Terrestrial Ecosystem Processes.” Ecology Letters 7 (8): 740–754. doi:10.1111/j.1461-0248.2004.00620.x.

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Wilson, G. W. T., C. W. Rice, M. C. Rillig, A. Springer, D. C. Hartnett, et al. 2009. “Soil Aggregation and Carbon Sequestration are Tightly Correlated with the Abundance of Arbuscular Mycorrhizal Fungi: Results from long-term Field Experiments.” . Ecology Letters 12 (5): 452–461. doi:10.1111/j.1461-0248.2009.01303.x.

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Khan, A. G. 2005. “Role of Soil Microbes in the Rhizospheres of Plants Growing on Trace Metal Contaminated Soils in Phytoremediation.” Journal of Trace Elements in Medicine and Biology 18 (4): 355–364. doi:10.1016/j.jtemb.2005.02.006.

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Rillig, M. C., S. F. Wright, K. A. Nichols, W. F. Schmidt, M. S. Torn, et al. 2001b. “Large Contribution of Arbuscular Mycorrhizal Fungi to Soil Carbon Pools in Tropical Forest Soils.” Plant and Soil 233 (2): 167–177. doi:10.1023/a:1010364221169.

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Rillig, M. C., S. F. Wright, and V. T. Eviner. 2002. “The Role of Arbuscular Mycorrhizal Fungi and Glomalin in Soil Aggregation: Comparing Effects of Five Plant Species.” Plant and Soil 238 (2): 325–333. doi:10.1023/a:1014483303813.

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Gonzalez-Chavez, M. C., R. Carrillo-Gonzalez, S. F. Wright, K. A. Nichols, et al. 2004. “The Role of Glomalin, a Protein Produced by Arbuscular Mycorrhizal Fungi, in Sequestering Potentially Toxic Elements.” Environmental Pollution 130 (3): 317–323. doi:10.1016/j.envpol.2004.01.004.

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Driver, J. D., W. E. Holben, and M. C. Rillig. 2005. “Characterization of Glomalin as a Hyphal Wall Component of Arbuscular Mycorrhizal Fungi.” Soil Biology and Biochemistry 37 (1): 101–106. doi:10.1016/j.soilbio.2004.06.011.

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Rillig, M. C., and P. D. Steinberg. 2002. “Glomalin Production by an Arbuscular Mycorrhizal Fungus: A Mechanism of Habitat Modification?” Soil Biology and Biochemistry 34 (9): 1371–1374. doi:10.1016/s0038-0717(02)00060-3.

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Riaz, M., M. Kamran, Y. Z. Fang, et al. 2021. “Arbuscular Mycorrhizal fungi-induced Mitigation of Heavy Metal Phytotoxicity in Metal Contaminated Soils: A Critical Review.” Journal of Hazardous Materials 402:15. doi:10.1016/j.jhazmat.2020.123919.

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Kumar, S., A. K. Singh, and P. Ghosh. 2018. “Distribution of Soil Organic Carbon and Glomalin Related Soil Protein in Reclaimed Coal mine-land Chronosequence under Tropical Condition.” Science of the Total Environment 625: 1341–1350. doi:10.1016/j.scitotenv.2018.01.061.

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Lovelock, C. E., S. F. Wright, D. A. Clark, R. W. Ruess, et al. 2004. “Soil Stocks of Glomalin Produced by Arbuscular Mycorrhizal Fungi across a Tropical Rain Forest Landscape.” Journal of Ecology 92 (2): 278–287. doi:10.1111/j.0022-0477.2004.00855.x.

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Gao, W. Q., P. Wang, and Q. S. Wu. 2019. “Functions and Application of Glomalin-Related Soil Proteins: A Review.” Sains Malaysiana 48 (1): 111–119. doi:10.17576/jsm-2019-4801-13.

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Agnihotri, R., M. P. Sharma, A. Prakash, A. Ramesh, S. Bhattacharjya, A. K. Patra, M. C. Manna, et al. 2022. “Glycoproteins of Arbuscular Mycorrhiza for Soil Carbon Sequestration: Review of Mechanisms and Controls.” Science of the Total Environment 806:150571. doi:10.1016/j.scitotenv.2021.150571.

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Singh, A. K., X. A. Zhu, C. F. Chen, et al. 2020. “The Role of Glomalin in Mitigation of Multiple Soil Degradation Problems.” Critical Reviews in Environmental Science and Technology 35. doi:10.1080/10643389.2020.1862561.

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Wu, Q. S., R. X. Xia, and Y. N. Zou. 2008. “Improved Soil Structure and Citrus Growth after Inoculation with Three Arbuscular Mycorrhizal Fungi under Drought Stress.” European Journal of Soil Biology 44 (1): 122–128. doi:10.1016/j.ejsobi.2007.10.001.

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Hammer, E. C., M. C. Rillig, and K. Nielsen. 2011. “The Influence of Different Stresses on Glomalin Levels in an Arbuscular Mycorrhizal Fungus-Salinity Increases Glomalin Content.” PLoS One 6 (12): 5. doi:10.1371/journal.pone.0028426.

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Vodnik, D., H. Grcman, I. Macek, J. T. van Elteren, M. Kovačevič, et al. 2008. “The Contribution of glomalin-related Soil Protein to Pb and Zn Sequestration in Polluted Soil.” . Science of the Total Environment 392 (1): 130–136. doi:10.1016/j.scitotenv.2007.11.016.

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