Abstract
Aims
Growers in northern U.S. regions rely on winter annual legume cover crop symbiotic nitrogen fixation (SNF) to reduce the need for spring fertilization and build soil organic matter. However, cold transitional fall temperatures potentially limit SNF. This study examined the effects of cold temperatures on nodulation and SNF in legume cover crops.
Methods
In a growth chamber experiment, hairy vetch (Vicia villosa Roth), Austrian winter pea (Pisum sativum L.) and crimson clover (Trifolium incarnatum L.) were sown in growth pouches, inoculated with rhizobia, and placed in growth chambers ranging from 5℃ to 20℃ for six weeks. In a field experiment, the same legumes were sown in fall, with destructive sampling at four time points from November to May. In both experiments, plant biomass, nodulation, and SNF was assessed.
Results
In the controlled environment, incrementally lower temperatures negatively affected legume cover crop biomass and nodulation parameters across all species, especially at 5 °C (41°F). Controlled environment results also suggest that optimum temperatures for SNF in cover crop legumes falls in the range of 15 °C to 20 °C. In the field, winter conditions negatively affected legume cover crop productivity, with plant biomass, nodule number, and nodule mass greatest in fall and spring, and lowest in winter. Hairy vetch had the best growth response to spring warming, suggesting it is well-suited to over-winter protected environment production. SNF also decreased during winter and failed to recover by spring cover crop termination.
Conclusions
Winter annual legume cover crops may not experience reduced growth, nodulation, or SNF until temperatures fall below 10℃; this estimate is lower than previously reported for cover crop legumes. These temperatures are typical of cover crop establishment periods, suggesting winter cover crop species selection is critical; the over-wintering performance of hairy vetch makes it a promising option for temperate regions.
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Abbreviations
- DAI:
-
Days after inoculation
- N:
-
Nitrogen
- SNF:
-
Symbiotic nitrogen fixation
References
Abdollahi L, Munkholm LJ (2014) Tillage system and cover crop effects on soil quality: I. Chemical, mechanical, and biological properties. Soil Sci Soc Am J 78:262. https://doi.org/10.2136/sssaj2013.07.0301
Alexandre A, Oliveira S (2013) Response to temperature stress in rhizobia. Crit Rev Microbiol 39:219–228
Baraibar B, Hunter MC, Schipanski ME et al (2018) Weed suppression in cover crop monocultures and mixtures. Weed Sci 66:121–133. https://doi.org/10.1017/wsc.2017.59
Bergersen FJ, Hely FW, Costin AB (1963) Overwintering of clover nodules in alpine conditions. Aust J Biol Sci 16:920–921
Bhandari K, Sharma KD, Hanumantha Rao B et al (2017) Temperature sensitivity of food legumes: a physiological insight. Acta Physiol Plant 39:68. https://doi.org/10.1007/s11738-017-2361-5
Blanco-Canqui H, Shaver TM, Lindquist JL et al (2015) Cover crops and ecosystem services: Insights from studies in temperate soils. Agron J 107:2449–2474. https://doi.org/10.2134/agronj15.0086
Blesh J (2018) Functional traits in cover crop mixtures: Biological nitrogen fixation and multifunctionality. J Appl Ecol 55:38–48. https://doi.org/10.1111/1365-2664.13011
Brandsæter LO, Smeby T, Tronsmo AM, Netland J (2000) Winter annual legumes for use as cover crops in row crops in northern regions: II. Frost resistance study. Crop Sci 40:175–181. https://doi.org/10.2135/cropsci2000.401175x
Brandsæter LO, Heggen H, Riley H et al (2008) Winter survival, biomass accumulation and N mineralization of winter annual and biennial legumes sown at various times of year in Northern Temperate Regions. Eur J Agron 28:437–448. https://doi.org/10.1016/j.eja.2007.11.013
Brandsaeter LO, Netland J (1999a) Winter annual legumes for use as cover crops in Northern Regions: 1. Field Experiments Crop Sci 39:1369–1379
Brandsaeter LO, Netland J (1999b) Winter annual legumes for use as cover crops in row crops in Northern Regions: 1. Field Experiments Crop Sci 39:1369–1379
Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080. https://doi.org/10.1042/bj1251075
Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372
Curran WS, Hoover RJ, Mirsky SB et al (2018) Evaluation of cover crops drill interseeded into corn across the mid-Atlantic region. Agron J 110:435–443. https://doi.org/10.2134/agronj2017.07.0395
Dakora FD (1995) A functional relationship between leghaemoglobin and nitrogenase based on novel measurements of the two proteins in legume root nodules. Ann Bot 75:49–54. https://doi.org/10.1016/S0305-7364(05)80008-3
Dehaghi MA, Sanavy SAMM (2003) Effect of root-zone temperatures on morphology, growth and development, yield, and yield components of annual medics. Aust J Agric Res 54:917–921. https://doi.org/10.1071/AR02067
Denison RF (2005) A Darwinian perspective on improving nitrogen-fixation efficiency of legume crops and forages, Second Edi. Elsevier Inc
Denison RF (2021) Legume-imposed selection for more-efficient symbiotic rhizobia. Proc Natl Acad Sci U S A 118:22–24. https://doi.org/10.1073/pnas.2107033118
Divito GA, Sadras VO (2014) How do phosphorus, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. F Crop Res 156:161–171. https://doi.org/10.1016/j.fcr.2013.11.004
Dobert RC, Blevins DG (1993) Effect of seed size and plant growth on nodulation and nodule development in lima bean (Phaseolus lunatus L.). Plant Soil 148:11–19. https://doi.org/10.1007/BF02185380
Duzan HM, Mabood F, Souleimanov A, Smith DL (2006) Nod Bj-V (C<inf>18:1</inf>, MeFuc) production by Bradyrhizobium japonicum (USDA110, 532C) at suboptimal growth temperatures. J Plant Physiol 163:107–111. https://doi.org/10.1016/j.jplph.2005.04.029
Everhart E, Hansen R, Lewis D et al (2010) Iowa High Tunnel Fruit and Vegetable Production Manual. 95
Ferguson BJ, Mens C, Hastwell AH et al (2019) Legume nodulation: the host controls the party. Plant Cell Environ 42:41–51
Gurusamy C, Davis P, Bal A (2000) Seasonal changes in perennial nodules of beach pea (Lathyrus maritimus Bigel.) with special reference to oleosomes. Int J Plant Sci 161:631–638
Hoagland DR, Arnon DI (1950) water culture methods for growing plants without soil. Calif Agric Exp Stn 32
Jett LW (2000) High Tunnel Temperature Management [Fact sheet]. U.S.D.A. Sustainable Agriculture Research and Education. https://www.sare.org/resources/high-tunnel-temperature-management/
Jones BC, Olson-Rutz K (2018) Inoculation and nitrogen management to optimize pulse crop yield and protein. Crop Soils 51:12–59
Kladivko EJ, Kaspar TC, Jaynes DB et al (2014) Cover crops in the upper midwestern United States : Potential adoption and reduction of nitrate leaching in the Mississippi River Basin. 69:279–291. https://doi.org/10.2489/jswc.69.4.279
Lawson A, Cogger C, Bary A, Fortuna AM (2015) Influence of seeding ratio, planting date, and termination date on rye-hairy vetch cover crop mixture performance under organic management. PLoS ONE 10:1–19. https://doi.org/10.1371/journal.pone.0129597
Liebman AM, Grossman J, Brown M et al (2018) Legume cover crops and tillage impact nitrogen dynamics in organic corn production. Agron J 110:1046–1057. https://doi.org/10.2134/agronj2017.08.0474
Lim CW, Lee YW, Lee SC, Hwang CH (2014) Nitrate inhibits soybean nodulation by regulating expression of CLE genes. Plant Sci 229:1–9. https://doi.org/10.1016/j.plantsci.2014.08.014
Lipsanen P, Lindström K (1986) Adaptation of red clover rhizobia to low temperatures. Plant Soil 92:55–62. https://doi.org/10.1007/BF02372266
Lira MA, Nascimento LRS, Fracetto GGM (2015) Legume-rhizobia signal exchange: promiscuity and environmental effects. Front Microbiol 6:1–9. https://doi.org/10.3389/fmicb.2015.00945
Lira Junior MDA, Lima AST, Arruda JRF, Smith DL (2005) Effect of root temperature on nodule development of bean, lentil and pea. Soil Biol Biochem 37:235–239. https://doi.org/10.1016/j.soilbio.2004.07.032
Magdoff F, van Es H (1993) Building Soils for Better Crops. Sustainable Agriculture Research and Education, College Park
Mahdavi B, Modarres Sanavy SAM, Saberali SF, Dolatabadian A (2010) Influence of root-zone temperature on growth and nitrogen fixation in three Iranian grasspea landraces. Acta Agric Scand Sect B Soil Plant Sci 60:40–47. https://doi.org/10.1080/09064710802609527
Malone RW, Jaynes DB, Kaspar TC et al (2014) Cover crops in the upper midwestern United States : simulated effect on nitrate leaching with artificial drainage. 69:292–305. https://doi.org/10.2489/jswc.69.4.292
Marrou H, Ricaurte JJ, Ghanem ME et al (2018) Is nitrogen accumulation in grain legumes responsive to growth or ontogeny? Physiol Plant 162:109–122. https://doi.org/10.1111/ppl.12617
Martin BGW, Touchton JT (1983) Legumes as a cover crop and source of nitrogen. J Soil Water Conserv 38:214–216
Maul J, Mirsky S, Emche S, Devine T (2011) Evaluating a germplasm collection of the cover crop hairy vetch for use in sustainable farming systems. Crop Sci 51:2615–2625. https://doi.org/10.2135/cropsci2010.09.0561
McCauley AM, Jones CA, Miller PR et al (2012) Nitrogen fixation by pea and lentil green manures in a semi-arid agroecoregion: effect of planting and termination timing. Nutr Cycl Agroecosystems 92:305–314. https://doi.org/10.1007/s10705-012-9491-3
Mendes IC, Bandick AK, Dick RP, Bottomley PJ (1999) Microbial biomass and activities in soil aggregates affected by winter cover crops. Soil Sci Soc Am J 63:1173–1179
Moncada K, Sheaffer C (2010) Winter Cover Crops. In: Risk Management Guide for Organic Producers. pp 1–22. https://organicriskmanagement.umn.edu
Mothapo NV, Grossman JM, Sooksa-nguan T et al (2013) Cropping history affects nodulation and symbiotic efficiency of distinct hairy vetch (Vicia villosa Roth.) genotypes with resident soil rhizobia. Biol Fertil Soils 49:871–879. https://doi.org/10.1007/s00374-013-0781-y
NOAA (2019) National Weather Service Forecast Office
NOAA-NCEI (2018) NOAA-NCEI. In: U.S. Rec
Ofosu-Budu KG, Ogata S, Fujita K (1992) Temperature effects on root nodule activity and nitrogen release in some sub-tropical and temperate legumes. Soil Sci Plant Nutr 38:717–726. https://doi.org/10.1080/00380768.1992.10416702
Parr M, Grossman JM, Reberg-Horton SC et al (2011) Nitrogen delivery from legume cover crops in no-till organic corn production. Agron J 103:1578–1590. https://doi.org/10.2134/agronj2011.0007
Perdigão A, Coutinho J, Moreira N (2012) Cover crops as nitrogen source for organic farming in southwest Europe. Acta Hortic 933:355–362
Perkus EA, Grossman JM, Avenue F et al (2022) Exploring overwintered cover crops as a soil management tool in upper-midwest high tunnels. HortScience 57:171–180. https://doi.org/10.21273/HORTSCI15987-21
Perkus E (2018) Legume cover crops in high tunnels: Field evaluation for soil health and controlled environment freezing tolerance. University of Minnesota
Perrone S, Grossman J, Liebman A et al (2020) Nitrogen fixation and productivity of winter annual legume cover crops in Upper Midwest organic cropping systems. Nutr Cycl Agroecosyst 117:61–76. https://doi.org/10.1007/s10705-020-10055-z
Pommeresche R, Hansen S (2017) Examining root nodule activity on legumes. FertilCrop Tech. Note 1–4
Poustini K, Mabood F, Smith DL (2005) Low root zone temperature effects on bean (Phaseolus vulgaris L.) plants inoculated with Rhizobium leguminosarum bv. phaseoli pre-incubated with methyl jasmonate and/or genistein. Acta Agric Scand Sect B-Soil Plant Sci 55:293–298. https://doi.org/10.1080/09064710500246127
Power JF, Zachariassen JA (1993) Relative nitrogen utilization by legume cover crop species at three soil temperatures. Agron J 85:134–140
Prévost D, Bromfield ESP (1991) Effect of low root temperature on symbiotic nitrogen fixation and competitive nodulation of Onobrychis viciifolia (sainfoin) by strains of arctic and temperate rhizobia. Biol Fertil Soils 12:161–164. https://doi.org/10.1007/BF00337195
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Rice WA, Olsen PE, Collins MM (1995) Symbiotic effectiveness of Rhizobium meliloti at low root temperature. Plant Soil 170:351–358
Robin C, Sultan-Tubeileh K, Obaton M, Guckert A (2005) Nitrogen fixation and growth of annual Medicago-Sinorhizobium associations at low temperature. Eur J Agron 22:267–275. https://doi.org/10.1016/j.eja.2004.04.001
Rütting T, Aronsson H, Delin S (2018) Efficient use of nitrogen in agriculture. Nutr Cycl Agroecosyst 110:1–5. https://doi.org/10.1007/s10705-017-9900-8
SARE, CTIC (2015) Cover Crop Survey Annual Report 2014–2015
Sato T (2014) Effects of Rhizobium Inoculation on Nitrogen Fixation and Growth of Leguminous Green Manure Crop Hairy Vetch (Vicia villosa Roth). In: Advances in Biology and Ecology of Nitrogen Fixation. pp 225–236. IntechOpen.
Schipanski ME, Drinkwater LE, Russelle MP (2010) Understanding the variability in soybean nitrogen fixation across agroecosystems. Plant Soil 329:379–397. https://doi.org/10.1007/s11104-009-0165-0
Scholberg JMS, Dogliotti S, Leoni C, Cherr CM, Zotarelli L, Rossing WAH (2010) Cover Crops for Sustainable Agrosystems in the Americas. In: Lichtfouse E (eds) Genetic Engineering, Biofertilisation, Soil Quality and Organic Farming. Sustainable Agriculture Reviews, vol 4. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-8741-6_2
Silsbury JH (1977) Energy requirement for symbiotic nitrogen fixation. Nature 267:149–150. https://doi.org/10.1038/267149a0
Snapp SS, Swinton SM, Labarta R et al (2005) Evaluating cover crops for benefits, costs and performance within cropping system niches. Agron J 97:322–332. https://doi.org/10.2134/agronj2005.0322a
Teasdale JR, Devine TE, Mosjidis JA et al (2004) Growth and development of hairy vetch cultivars in the northeastern United States as influenced by planting and harvesting date. Agron J 96:1266–1271. https://doi.org/10.2134/agronj2004.1266
Unkovich MJ, Baldock J, Peoples MB (2010) Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes. Plant Soil 329:75–89. https://doi.org/10.1007/s11104-009-0136-5
Unkovich M, Herridge D, Peoples M et al (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Austrailian Cent Int Agric Res: 1–258. https://doi.org/10.1071/AR9940119
USDA-AMS (2018) Organic Foods Production Act Provisions Part 205 — National Organic Program
USDA-NASS (2012) 2012 Census of Agriculture - United States Summary and State Data
van Heerden PDR, Kruger GHJ (2004) Dark chilling inhibition of photosynthesis and symbiotic nitrogen fixation in soybean during pod filling. J Plant Physiol 161:599–609. https://doi.org/10.1078/0176-1617-01114
Voisin AS, Salon C, Munier-Jolain NG, Ney B (2002) Quantitative effects of soil nitrate, growth potential and phenology on symbiotic nitrogen fixation of pea (Pisum sativum L.). Plant Soil 243:31–42. https://doi.org/10.1023/A:1019966207970
Wade T, Claassen R, Wallander S (2015) Conservation-Practice Adoption Rates Vary Widely by Crop and Region United States Department of Agriculture
Ward MJ, Bomford MK (2013) Row covers moderate diurnal temperature flux in high tunnels. Acta Hortic 987:59–66
Wayman S, Kissing Kucek L, Mirsky SB et al (2017) Organic and conventional farmers differ in their perspectives on cover crop use and breeding. Renew Agric Food Syst 32:376–385. https://doi.org/10.1017/S1742170516000338
Wery J, Silim SN, Knights EJ et al (1994) Screening techniques and sources of tolerance to extremes of moisture and air temperature in cool season food legumes. Euphytica 73:73–83. https://doi.org/10.1007/BF00027185
Wiering NP, Flavin C, Sheaffer CC et al (2018) Winter hardiness and freezing tolerance in a hairy vetch collection. Crop Sci 58:1594–1604. https://doi.org/10.2135/cropsci2017.12.0748
Wilke BJ, Snapp SS (2008) Winter cover crops for local ecosystems : linking plant traits and ecosystem function. J Sci Food Agric 88:551–557. https://doi.org/10.1002/jsfa
Young-Matthews A (2017) Cover crop variety adaptation trials in Corvallis, OR [Annual Progress Report]. USDA NRCS. https://www.nrcs.usda.gov/Internet/FSE_PLANTMATERIALS/publications/orpmcot13159.pdf
Zhang F, Lynch DH, Smith DL (1995) Impact of low root temperatures in soybean [Glycine max. (L.) Merr.] on nodulation and nitrogen fixation. Environ Exp Bot 35:279–285. https://doi.org/10.1016/0098-8472(95)00017-7
Zhang F, Dijak M, Smith DL et al (1997) Nitrogen fixation and nitrate metabolism for growth of six diverse soybean [Glycine max. (L.) Merr.] genotypes under low temperature stress. Environ Exp Bot 38:49–60. https://doi.org/10.1016/S0098-8472(96)01053-2
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We thank the Organic Agriculture Research and Extension Initiative project 2015-2018 (Award #2015-51300-24192) for funding to complete this project.
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The authors have no relevant financial or non-financial interests to disclose. All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Charlotte Thurston. The first draft of the manuscript was written Charlotte Thurston, with a significantly revised draft written by Rebecca Fudge and Julie Grossman. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Thurston, C.L., Grossman, J.M., Fudge, R. et al. Cold stress reduces nodulation and symbiotic nitrogen fixation in winter annual legume cover crops. Plant Soil 481, 661–676 (2022). https://doi.org/10.1007/s11104-022-05667-z
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DOI: https://doi.org/10.1007/s11104-022-05667-z