Current IssueEditorial BoardOnline First ArticlesArchive
Current IssueEditorial BoardOnline First ArticlesArchive

Review Article

Thermal Sensitivity of Legume-rhizobium Interactions: Root Morphogenesis and Variability: A Review

M
M Panchulakshmi1
https://orcid.org/0009-0001-6227-3720
D
Dheebakaran Ga1,*
https://orcid.org/0000-0002-0603-192X
N
N.K. Sathyamoorthy1
https://orcid.org/0000-0002-7296-4808
D
D. Jegadeeswari2
https://orcid.org/0000-0002-2806-8280
B
B. Arthirani3
https://orcid.org/0000-0002-1651-3922
M
M. Dhasarathan1
https://orcid.org/0000-0002-9192-4430
S
S. Mohan Kumar1
https://orcid.org/0000-0002-2301-438X
1Agro Climate Research Centre, Tamil Nadu Agricultural University, Coimbatore-641 003, Tamil Nadu, India.
2Soil Science and Agricultural Chemistry, Tamil Nadu Agricultural University, Coimbatore-641 003, Tamil Nadu, India.
3Agricultural Research Station, Tamil Nadu Agricultural University, Kovilpatti-628 501, Tamil Nadu, India.

  • Submitted24-11-2025|

  • Accepted13-02-2026|

  • First Online 05-03-2026|

  • doi 10.18805/LR-5609

ABSTRACT

Legumes are vital to food and nutritional security, often referred to as the “poor man’s meat” because of their high protein content. Their role in sustainable agriculture is anchored in Biological Nitrogen Fixation (BNF), a symbiotic process involving rhizobia that is highly sensitive to fluctuation in soil temperature. Soil temperature governs root system architecture (RSA), microbial colonization and enzymatic activity and is a critical determinant of legume productivity. Extreme soil temperatures impair root activity, microbial symbiosis and nitrogen fixation. This synthesis drew from over 91 out of 124 peer-reviewed studies spanning molecular biology, microbial ecology and agronomic interventions. It examines temperature thresholds affecting nodulation kinetics, RSA traits and symbiotic gene expression, including heat shock proteins (HSPs), cold responsive genes (e.g., GmFRI-1) and hormonal signalling pathways. RSA traits such as root elongation, branching, biomass and vascular development are temperature sensitive, with optimal performance between 20-30oC. Cold stress delays nodulation and reduces nitrogenase activity (~60% at 4oC), while heat stress damages root tip and reduces nitrogenase reductase (~42%). Molecular responses include disrupted auxin transport and HSP induction. Thermotolerant rhizobial strains, Nod factors and inoculation strategies support symbiosis. Agronomic practices such as mulching, conservation tillage and strategic sowing buffer soil thermal regimes and enhance microbial activity. Managing the thermal sensitivity of the legume-rhizobium system through integrated genetic, microbial and agronomic strategies are vital for climate resilient legume cultivation and sustained productivity under variable soil temperature regimes.

INTRODUCTION

Legumes play a pivotal role in food and nutritional security, especially in low-income and vegetarian populations, earning the moniker “poor man’s meat” due to their protein, essential amino acids and affordability. Rich in micronutrients like iron, zinc and folate, contribute to balanced diets and combat hidden hunger. Agronomically, legumes sustain farming systems through biological nitrogen fixation (BNF), wherein symbiotic rhizobia convert atmospheric nitrogen into plant-available forms, reducing fertilizer dependency and enhancing soil fertility (Wissal et al., 2020; Owaresat et al., 2023). Their dual roles in nutrition and agro-ecological resilience makes legumes central to climate-smart agriculture and inclusive food systems.
 
Global and regional legume crops in food security
 
Legumes have diverse global centres of origin, reflecting their ancient domestication across continents. Chickpea and Lentil were domesticated in the Fertile Crescent (Zohary et al., 2012). Peas traces its roots to the Mediterranean Basin and Central Asia. Soybean originated in northeastern China  (Hymowitz and Shurtleff, 2005). The common bean has dual centres in Mesoamerica and the Andean region of South America (Bellucci et al., 2013), while Faba bean originated in the Near East, although its wild progenitor remains unidentified (Caracuta et al., 2016). Groundnut is native to South America, particularly Brazil and Peru (Krapovickas, 2017). Cowpea emerged from Sub-Saharan Africa, adapted to arid climates and low-input systems (Boukar et al., 2019). Grass pea, known for its drought tolerance, is native to the Mediterranean and South Asia (Gonçalves et al., 2024). India is a major centre of origin for several tropical legumes such as pigeon pea, black gram, green gram, Horse Gram, Lablab Bean and Moth Bean are native to the Indian subcontinent, where they have long supported rainfed subsistence farming and protein nutrition (Srivastava et al., 2025). These origins underscore the ecological and cultural significance of legumes in shaping resilient food systems across agro climatic zones in India.
       
Leguminosae crops addresses global food and nutritional security challenges, particularly in regions with protein-deficient diets (Salaria et al., 2022; Amel et al., 2018), being rich in protein (20-35%) (Grdeñ and Jakubczyk, 2023), essential amino acids, fibre, vitamins and minerals (Cakir et al., 2019). Legumes offer a nutritionally balanced alternative to animal protein (Rajput et al., 2024), make them especially valuable in vegetarian populations in India, where pulses are dietary stables. Globally, rising demand for plant-based proteins reflects health and sustainability concerns (Aschemann-Witzel et al., 2021).
       
Legumes like lentils, chickpeas, mung beans and soybeans are recognized as “future-smart foods” for their nutritional and ecological resilience (Sharma et al., 2024). In India, pulses contribute significantly to protein intake and are culturally embedded in rural traditional food systems (Singh et al., 2017; Sonika et al., 2020). Beyond human nutrition, legumes also support sustainable diets by reducing reliance on resource-intensive animal agriculture (Röös et al., 2020). Their inclusion in cropping systems enhances food system diversity and resilience, align with the UN Sustainable Development Goals (SDGs), particularly SDG 2 (Zero Hunger) and SDG 13 (Climate Action) (Unicef, 2022).
       
Despite their benefits, legume production is constrained by low yields, biotic and abiotic stresses and limited policy support. Breeding, biofortification and value addition are key to enhancing their role in global food and nutritional security worldwide.
 
Objective and scope of the review
 
This review synthesizes current knowledge on soil temperature effects on legume rhizobium interactions, with emphasis on root morphogenesis and nitrogen dynamics across physiological, molecular, microbial and agronomic dimensions relevant to climate resilient cultivation. The process is illustrated in the graphical abstract (Fig 1) and PRISMA flow diagram (Fig 2).

Fig 1: System of literature review process adopted in this review article.



Fig 2: PRISMA flow diagram.


       
From an initial 162 publications retrieved via Scopus, Web of Science, Google Scholar, PubMed and CAB Abstracts using targeted keywords, 124 were shortlisted after screening and 91 peer-reviewed studies were retained for final synthesis, based on rigor and relevance.
       
Thematic organization focused on temperature thresholds influencing nodulation, root system architecture (RSA) and symbiotic gene expression. Key regulators included heat shock proteins, cold responsive genes (e.g., GmFRI-1) and hormonal pathways modulating auxin-cytokinin dynamics. Integrated analysis covered physiological traits (root elongation, branching, biomass), microbial adaptations (strain tolerance, inoculant formulations) and agronomic practices (mulching, conservation tillage, co-inoculation) that shape symbiotic efficiency under variable soil temperatures.
 
Soil temperature and crop production
 
Soil temperature is a fundamental environmental variable regulating biological, chemical and physical processes in agriculture. It directly influences seed germination, root development, microbial activity, nutrient mineralization and water uptake, making it a critical determinant of crop productivity (Hatfield and Prueger, 2015). Optimal soil temperatures for tropical and subtropical crops are typically 20-30oC, varying by species and growth stage. Deviations from this range due to seasonal or climate induced shifts can disrupt enzymatic activity and hormonal signalling, impairing seed imbibition, radicle emergence and root elongation. (Yanjun et al., 2005). Cold soils delay germination and weaken seedling vigour, while excessive warmth accelerates metabolism but impairs root integrity and water balance. Nutrient solubility and uptake is also affected, with phosphorus availability reduced in cooler soils due to limited microbial activity (Blackwell et al., 2010). Microbial processes like decomposition, nitrification and symbiosis are highly temperature sensitive, shaping microbial biomass, diversity and nutrient cycling.
       
Conservation practices such as mulching, cover cropping and residue management help maintain optimal thermal regimes for microbial health and crop resilience (Lal, 2020). Moreover, soil temperature interacts with moisture dynamics, influencing evapotranspiration, root water uptake and drought tolerance. Recent studies highlight its role in regulating enzymatic activity, membrane fluidity and hormonal signalling, affecting germination, root growth and biomass accumulation  (Yeremko et al., 2025).
       
Understanding soil temperature dynamics is crucial for optimizing legume productivity, guiding sowing windows, varietal choice and inoculant strategies for climate resilient agriculture. While warmer soils may extend temperate growing seasons but also intensify heat stress and disrupt root–microbe interactions in tropical zones. A nuanced grasp of these dynamics is essential for designing adaptive agronomic practices, selecting thermotolerant cultivars and refining sowing schedules under variable climates.
 
Root system architecture under soil temperature stress
 
The rhizosphere is highly sensitive to temperature fluctuations, especially in legumes where root-microbe interactions drive productivity. Soil temperature shapes root system architecture (RSA), influencing elongation, branching and biomass (Luo et al., 2020). RSA governs water and nutrient uptake, microbial colonization and stress resilience. A dual fertilizing layer at the 30/ cm crest buffers soil temperature, enhancing root geometry through shallower angles, lateral proliferation, increased diameter and vertical expansion (Kang et al., 2025). Conversely, cooler root zones (7-13oC) restrict root growth and reduce vascular duct size, impairing mineral uptake and translocation (Miao et al., 2023).
 
Root elongation
 
Highly temperature sensitive, elongation in soybean peaks near 30oC, while drops by 70% at 12oC (de Moraes and Gusmao, 2021). Near-zero temperatures halted root extension in cereals like wheat and maize (Morandage et al., 2021), while cooler soils reduce root length density in spring cereals, limiting soil exploration (Qin et al., 2018). Most legumes elongate optimally 20-28oC; below 15oC, cell division slows, while above 35oC root tips are damaged, reducing elongation and lateral root formation.
 
Lateral root formation
 
Moderate soil warmth promoting auxin-mediated lateral root development, while excessive heat disrupts hormonal signalling, producing sparse roots. Tripathi et al. (2024) reported that legumes exposed to fluctuating soil temperatures exhibited altered branching patterns and reduced adventitious root density, impairing nodulation and nitrogen fixation.
 
Biomass accumulation
 
Root biomass peaks under optimal soil temperature and moisture. Legumes showed higher root biomass cooler temperatures (19-20oC), due to improved water retention and reduced thermal stress (Tchapga et al., 2023). Elevated temperatures accelerate decomposition but reduce biomass via increased respiration and lower carbon allocation. In maize, root dry weight was highest under 30/22oC and 35/27oC regimes (Walne and Reddy, 2022), while warming 4-6oC above ambient deteriorated fine roots and reduce absorptive root biomass (Parts et al., 2019). In cold ecosystems, warming increased root, fungal and fungivore biomass, though bacterial and archaeal levels remained stable (Salazar et al., 2020).
 
Thermal sensitivity of rhizobial function
 
Rhizobial activity and colonization under soil temperature stress
 
Soil temperature is a critical determinant of rhizobial activity, colonization efficiency and legume-rhizobium symbiosis. Rhizobia exhibit optimal metabolic activity and BNF between 20-30oC (Bordeleau and Prévost, 1994), while below 15oC or above 35oC impair bacterial viability, signal exchange and symbiotic function. Low temperatures slow rhizobial metabolism, reduce Nod factor synthesis and delay colonization (Liu et al., 2019). Cold stress also alters gene expression in rhizobia and host roots, affecting early signalling and nodule initiation. In contrast, elevated temperatures may boost root growth but disrupt rhizobial membrane integrity, enzymatic stability and signalling molecule production (Kumar et al., 2023; Caruso et al., 2014).
       
Soil temperature strongly influences rhizobial motility, chemotaxis and attachment to root hairs, critical steps for colonization. Moderate warmth enhances these processes and boosts nodule biomass, while temperatures outside the optimal (20-30oC) delay colonization (Zhang et al., 2020). Optimal temperatures (20-30oC) favour rhizobial colonization, nodule development and nitrogenase efficiency. Conversely, temperatures below 15oC or above 30oC can hinder nodulation and reduce nitrogen fixation rates (Aranjuelo et al., 2007; Mohammadi et al., 2012). Importantly, rhizobial strains vary in thermal tolerance, with some maintaining symbiotic efficiency under heat stress, making their selection vital for legume cultivation in warming climates  (Asadi Rahmani et al., 2009; Alexandre and Oliveira, 2011).
 
Rhizobial inoculant formulation and delivery systems
 
The efficacy of rhizobial inoculants under temperature stress depends on both strain selection and formulation. Carrier-based inoculants using peat, lignite, or charcoal help buffer rhizobia against desiccation and thermal fluctuations, extending shelf life and field viability (Bashan et al., 2014). Liquid inoculants enriched with protective polymers and osmolytes enhance thermal tolerance and rapid colonization, especially in high-temperature environments (Tittabutr et al., 2007). Encapsulation in alginate beads or biochar matrices creates protective microenvironments that moderate temperature and moisture stress  (Schoebitz and López Belchí, 2016). Precision placement of inoculants near the rhizosphere, particularly in mulched or conservation tillage systems, enhances nodulation. Combining thermotolerant strains with optimized formulations and targeted delivery sustains symbiosis under climate variability.
 
Molecular mechanisms of nodule initiation
 
Nodule formation begins with molecular dialogue between host roots and compatible rhizobia. Within nodules, rhizobia differentiate into nitrogen-fixing Bacteroides (Ledermann et al., 2021), supported by spatially and temporally regulated signalling networks. Nodules create a microaerobic niche for nutrient exchange and nitrogenase activity. Soil temperature influences nodule development and rhizobial strain competitiveness, for instance, B. diazoefficiens USDA 110/122 perform best at 28/23oC, while B. japonicum USDA 123 prefers cooler conditions (Shiro et al., 2016). Maintaining optimal soil temperatures and using thermotolerant strains with suitable soil management enhances symbiotic efficiency and legume productivity.
 
Thermal sensitivity of rhizobial function
 
Soil temperature on nodule formation
 
Rhizobia form a symbiotic association with legumes, enabling atmospheric nitrogen fixation through nodule formation (Masson-Boivin and Sachs, 2018; Raza et al., 2020). The process begins with root-exuded flavonoids that attract compatible rhizobia and induce Nod factor synthesis (Abd-Alla et al., 2023). These signals recognized by root surface receptors, triggering root hair curling and infection thread formation  (Krönauer and Radutoiu, 2021; Ghantasala and Roy Choudhury, 2022). Soil temperature critically influences rhizobial strain competitiveness and nodule occupancy. For example, B. diazoefficiens USDA 110/122 nodulated optimally at 28/23oC, while B. japonicum USDA 123 prefers cooler conditions, highlighting the importance of temperature-specific strain selection  (Shiro et al., 2016).
 
Temperature effects on nodule development
 
Optimal root-zone temperatures for nodule development are species-specific: 25oC for tropical beans, 20oC for peas and 15oC for lentils (Junior et al., 2005). Deviations delay nodule initiation and reduce size, number and growth rate. Rhizobial colonization also varies with temperature, rhizosphere populations rise between 20-30oC, while endophytic movement in chickpea peaks at 25oC (Landa et al., 2004). Co-inoculation with Bradyrhizobium and Azospirillum brasilense enhances nodulation in soybean under 20-30oC, with peak efficiency at 76% soil water retention and 112 nodules per plant (Deak et al., 2019). In contrast, low temperatures (15oC) reduce clover productivity and delay nodulation (Janczarek et al., 2024),  while high temperatures (>40oC) can cause nodulation failure and genetic stress in rhizobia (Hungria and Vargas, 2000).
 
Role of heat shock proteins in nodule development
 
In legumes, Heat shock proteins (HSPs) are essential for symbiosis during nodule development, preventing protein aggregation and maintaining cellular homeostasis (Ogden et al., 2017; Flynn et al., 2024). Small HSPs like GmHSP17.9 inhibit thermal aggregation of malate dehydrogenase at 45oC and support early signalling and differentiation  (Yang et al., 2022). HSPs also safeguard nitrogenase enzymes from heat-induced denaturation and oxidative stress, preserving nitrogen fixation (Rajaram and Apte, 2008). Heat-tolerant rhizobial strains such as CIAT899 upregulate specific HSPs (e.g., 21/ kDa) under 40-45oC, enhancing thermotolerance (Michiels et al., 1994). Their stress-induced expression makes HSPs valuable biomarkers and breeding targets for heat-resilient legumes, supporting symbiotic efficiency under climate stress (Aranjuelo et al., 2015).
 
Cold responsive genes and their impact on nodulation
 
Cold responsive genes enable legumes to sustain symbiosis under low-temperature stress by encoding proteins such as C-repeat binding factors (CBFs), antifreeze proteins and Osmo protectant enzymes that preserve cellular homeostasis  (Thomashow, 2010). Active rhizobial symbiosis enhances cold tolerance in alfalfa by boosting antioxidant defences and modulating cold-response genes (Liu et al., 2019). Cold stress disrupts hormonal signalling, cytokinin is pivotal for Nod factor transduction and nodule organogenesis (Dolgikh et al., 2016), while low temperatures suppress auxin transporters (PIN1-PIN7), impairing root elongation and gravitropism (Tiwari et al., 2023).  Nitrogenase activity is highly cold-sensitive, declining by 60% in Bradyrhizobium japonicum nodules within 24 hours at 4oC  (Zhang et al., 2014). However, genes like GmFRI-1 help maintain nodulation under cold stress, its overexpression enhances soyabean nodule formation at 4oC, while RNAi silencing inhibits it (Zhang et al., 2025).
 
Nodule senescence under temperature stress
 
Root nodule senescence is an orchestrated process involving the programmed death of bacteroids and plant cells, which results in a gradual decline in nitrogen fixation (Tsyganova et al., 2023). Temperature strongly shapes senescence, at 28oC, wild-type SGE nodules senesced centrally after three days, while mutant lines SGEFix”-3 and SGEFix”-7 showed rapid apex and basal senescence within one day  (Serova et al., 2023a). Heat-induced senescence is also governed by hormonal pathways, with upregulation of GA deactivation (PsGA2ox1), ethylene (PsACS2, PsACO1), jasmonic acid (PsLoxN1) and ABA synthesis genes (PsNCED2, PsAO3), alongside downregulation of GA biosynthesis gene PsGA20ox1-collectively promsoting nodule aging (Serova et al., 2023b).
 
Nitrogen fixation dynamics under soil temperature variability
 
Biological nitrogen fixation (BNF) is highly soil temperature-sensitive with extremes threaten symbiotic efficiency and crop productivity (Flynn et al., 2024; Kajić et al., 2016). Conservation tillage enhances nodulation and BNF by improving moisture retention, moderating temperature and boosting microbial biomass (Torabian et al., 2019). Root-zone temperature (RZT) is critical, nitrogen fixation in grass pea halts below 10oC, temperate rhizobia peak at 25oC and cold-adapted strains at 15oC (Mahdavi et al., 2010). This highlights the importance of matching rhizobial thermal adaptation to local soil conditions. In Arctic soils, BNF peaks below 14oC with adequate moisture, suggesting vulnerability of cold-adapted diazotrophs to warming (Rousk et al., 2018). In temperate zones, BNF rates rise with temperature, peaking at 35oC under moderate moisture (Li et al., 2018). In chickpea, nitrogenase and nitrate reductase activities peak during flowering but decline at ~39oC, with nitrogenase reductase dropping by 40.12% and nitrogenase by 20.21% (Jain et al., 2014). Ammonium assimilation enzymes GS and GOGAT are even more sensitive to heat stress (Hungria and Kaschuk, 2014). These findings highlight the critical need for temperature resilient symbiotic systems to sustain BNF under climate stress. The interactions between soil temperature and key activities in legume-rhizobium systems are summarized in Table 1 and a graphical abstract (Fig 3).

Table 1: Optimal soil temperature for the key activities in legume-rhizobium systems.



Fig 3: Graphical abstract of soil temperature and legume-rhizobium symbiosis.


 
Agronomic and microbial interventions for soil temperature management
 
Soil temperature regulates seed germination, root development, microbial activity and nutrient cycling, making its management vital under climate variability. Mulching with straw, leaf litter, or green manures, buffers temperature, conserves moisture and promotes microbial health. In Indian natural farming, mulching synergizes with inputs like Jeevamrit and Bijamrut to enhance nutrient cycling and nitrogen fixation (Lakhani and Bodar, 2025). Mulching also suppresses weeds, reduces evapotranspiration and cold stress, making it especially valuable in dryland and semi-arid regions (Demo and Asefa Bogale, 2024).
       
Thermotolerant strains of Rhizobium, Azospirillum and phosphate-solubilizing bacteria improve nodulation and nutrient uptake. Inoculants applied with organic carriers and placed near the root zone, often alongside mulching enhance microbial efficacy (Abro et al., 2011). Region-specific formulations are increasingly recommended to match local soils and cropping systems. Sowing window optimization-based on soil temperature thresholds improves germination and seedling vigour. Aligning sowing with seasonal rainfall and temperature patterns boosts yields (Zhang et al., 2019). Longterm Agrometeorological data and crop-weather calendars guide ideal sowing periods for rainfed crops.
       
Together, these interventions form a low-cost, synergistic framework for climate-resilient agriculture across diverse agro-climatic zones. Integrated with conservation agriculture and ICT-based advisories, they strengthen soil health, microbial diversity and crop productivity under temperature stress.
 
Way forward
 
To enhance legume productivity and nitrogen fixation under variable soil temperatures, integrated agronomic management strategies are essential to improve resilience. Advanced inoculant technologies, including encapsulated and polymer-enriched formulations may strengthen the nodulation process. Molecular insights into heat shock proteins, cold-responsive genes and hormonal pathways provide breeding targets. Embedding these approaches in extension programs, policies and farmer training ensures scalable adoption across diverse agro-climatic zones.

CONCLUSION

Soil temperature critically shapes root architecture and legume-rhizobium symbiosis, influencing water uptake, nutrient acquisition and nitrogen fixation. Extreme heat or cold impair root development and symbiotic efficiency. Integrating thermotolerant rhizobial strains, optimized inoculants, mulching and conservation tillage helps buffer temperature stress. Strategic sowing windows and root-zone management further enhance nodulation in rainfed systems. Molecular insights into heat shock proteins and cold-responsive genes offer new breeding targets for thermal resilience. Coupled with ICT-based advisories and region-specific agrometeorological data, these interventions can boost legume productivity and soil health. A systems approach, linking genetic, microbial and agronomic innovations is essential for sustaining biological nitrogen fixation and advancing climate-smart agriculture.

ACKNOWLEDGEMENT

The authors gratefully acknowledge the Ministry of Social Justice and Empowerment and the University Grants Commission (UGC), Government of India, for the student fellowship and sincerely thank the scientists of the DST–Centre of Excellence on Disaster and Climate Resilient Agriculture, Agro Climate Research Centre, TNAU, Coimbatore, for valuable support in collecting review materials.
 
Disclaimers
 
The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect loss resulting from the use of this content.
 
Informed consent
 
No animal used during the research.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

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    Review Article

    Thermal Sensitivity of Legume-rhizobium Interactions: Root Morphogenesis and Variability: A Review

    M
    M Panchulakshmi1
    https://orcid.org/0009-0001-6227-3720
    D
    Dheebakaran Ga1,*
    https://orcid.org/0000-0002-0603-192X
    N
    N.K. Sathyamoorthy1
    https://orcid.org/0000-0002-7296-4808
    D
    D. Jegadeeswari2
    https://orcid.org/0000-0002-2806-8280
    B
    B. Arthirani3
    https://orcid.org/0000-0002-1651-3922
    M
    M. Dhasarathan1
    https://orcid.org/0000-0002-9192-4430
    S
    S. Mohan Kumar1
    https://orcid.org/0000-0002-2301-438X
    1Agro Climate Research Centre, Tamil Nadu Agricultural University, Coimbatore-641 003, Tamil Nadu, India.
    2Soil Science and Agricultural Chemistry, Tamil Nadu Agricultural University, Coimbatore-641 003, Tamil Nadu, India.
    3Agricultural Research Station, Tamil Nadu Agricultural University, Kovilpatti-628 501, Tamil Nadu, India.

    • Submitted24-11-2025|

    • Accepted13-02-2026|

    • First Online 05-03-2026|

    • doi 10.18805/LR-5609

    ABSTRACT

    Legumes are vital to food and nutritional security, often referred to as the “poor man’s meat” because of their high protein content. Their role in sustainable agriculture is anchored in Biological Nitrogen Fixation (BNF), a symbiotic process involving rhizobia that is highly sensitive to fluctuation in soil temperature. Soil temperature governs root system architecture (RSA), microbial colonization and enzymatic activity and is a critical determinant of legume productivity. Extreme soil temperatures impair root activity, microbial symbiosis and nitrogen fixation. This synthesis drew from over 91 out of 124 peer-reviewed studies spanning molecular biology, microbial ecology and agronomic interventions. It examines temperature thresholds affecting nodulation kinetics, RSA traits and symbiotic gene expression, including heat shock proteins (HSPs), cold responsive genes (e.g., GmFRI-1) and hormonal signalling pathways. RSA traits such as root elongation, branching, biomass and vascular development are temperature sensitive, with optimal performance between 20-30oC. Cold stress delays nodulation and reduces nitrogenase activity (~60% at 4oC), while heat stress damages root tip and reduces nitrogenase reductase (~42%). Molecular responses include disrupted auxin transport and HSP induction. Thermotolerant rhizobial strains, Nod factors and inoculation strategies support symbiosis. Agronomic practices such as mulching, conservation tillage and strategic sowing buffer soil thermal regimes and enhance microbial activity. Managing the thermal sensitivity of the legume-rhizobium system through integrated genetic, microbial and agronomic strategies are vital for climate resilient legume cultivation and sustained productivity under variable soil temperature regimes.

    INTRODUCTION

    Legumes play a pivotal role in food and nutritional security, especially in low-income and vegetarian populations, earning the moniker “poor man’s meat” due to their protein, essential amino acids and affordability. Rich in micronutrients like iron, zinc and folate, contribute to balanced diets and combat hidden hunger. Agronomically, legumes sustain farming systems through biological nitrogen fixation (BNF), wherein symbiotic rhizobia convert atmospheric nitrogen into plant-available forms, reducing fertilizer dependency and enhancing soil fertility (Wissal et al., 2020; Owaresat et al., 2023). Their dual roles in nutrition and agro-ecological resilience makes legumes central to climate-smart agriculture and inclusive food systems.
     
    Global and regional legume crops in food security
     
    Legumes have diverse global centres of origin, reflecting their ancient domestication across continents. Chickpea and Lentil were domesticated in the Fertile Crescent (Zohary et al., 2012). Peas traces its roots to the Mediterranean Basin and Central Asia. Soybean originated in northeastern China  (Hymowitz and Shurtleff, 2005). The common bean has dual centres in Mesoamerica and the Andean region of South America (Bellucci et al., 2013), while Faba bean originated in the Near East, although its wild progenitor remains unidentified (Caracuta et al., 2016). Groundnut is native to South America, particularly Brazil and Peru (Krapovickas, 2017). Cowpea emerged from Sub-Saharan Africa, adapted to arid climates and low-input systems (Boukar et al., 2019). Grass pea, known for its drought tolerance, is native to the Mediterranean and South Asia (Gonçalves et al., 2024). India is a major centre of origin for several tropical legumes such as pigeon pea, black gram, green gram, Horse Gram, Lablab Bean and Moth Bean are native to the Indian subcontinent, where they have long supported rainfed subsistence farming and protein nutrition (Srivastava et al., 2025). These origins underscore the ecological and cultural significance of legumes in shaping resilient food systems across agro climatic zones in India.
           
    Leguminosae crops addresses global food and nutritional security challenges, particularly in regions with protein-deficient diets (Salaria et al., 2022; Amel et al., 2018), being rich in protein (20-35%) (Grdeñ and Jakubczyk, 2023), essential amino acids, fibre, vitamins and minerals (Cakir et al., 2019). Legumes offer a nutritionally balanced alternative to animal protein (Rajput et al., 2024), make them especially valuable in vegetarian populations in India, where pulses are dietary stables. Globally, rising demand for plant-based proteins reflects health and sustainability concerns (Aschemann-Witzel et al., 2021).
           
    Legumes like lentils, chickpeas, mung beans and soybeans are recognized as “future-smart foods” for their nutritional and ecological resilience (Sharma et al., 2024). In India, pulses contribute significantly to protein intake and are culturally embedded in rural traditional food systems (Singh et al., 2017; Sonika et al., 2020). Beyond human nutrition, legumes also support sustainable diets by reducing reliance on resource-intensive animal agriculture (Röös et al., 2020). Their inclusion in cropping systems enhances food system diversity and resilience, align with the UN Sustainable Development Goals (SDGs), particularly SDG 2 (Zero Hunger) and SDG 13 (Climate Action) (Unicef, 2022).
           
    Despite their benefits, legume production is constrained by low yields, biotic and abiotic stresses and limited policy support. Breeding, biofortification and value addition are key to enhancing their role in global food and nutritional security worldwide.
     
    Objective and scope of the review
     
    This review synthesizes current knowledge on soil temperature effects on legume rhizobium interactions, with emphasis on root morphogenesis and nitrogen dynamics across physiological, molecular, microbial and agronomic dimensions relevant to climate resilient cultivation. The process is illustrated in the graphical abstract (Fig 1) and PRISMA flow diagram (Fig 2).

    Fig 1: System of literature review process adopted in this review article.



    Fig 2: PRISMA flow diagram.


           
    From an initial 162 publications retrieved via Scopus, Web of Science, Google Scholar, PubMed and CAB Abstracts using targeted keywords, 124 were shortlisted after screening and 91 peer-reviewed studies were retained for final synthesis, based on rigor and relevance.
           
    Thematic organization focused on temperature thresholds influencing nodulation, root system architecture (RSA) and symbiotic gene expression. Key regulators included heat shock proteins, cold responsive genes (e.g., GmFRI-1) and hormonal pathways modulating auxin-cytokinin dynamics. Integrated analysis covered physiological traits (root elongation, branching, biomass), microbial adaptations (strain tolerance, inoculant formulations) and agronomic practices (mulching, conservation tillage, co-inoculation) that shape symbiotic efficiency under variable soil temperatures.
     
    Soil temperature and crop production
     
    Soil temperature is a fundamental environmental variable regulating biological, chemical and physical processes in agriculture. It directly influences seed germination, root development, microbial activity, nutrient mineralization and water uptake, making it a critical determinant of crop productivity (Hatfield and Prueger, 2015). Optimal soil temperatures for tropical and subtropical crops are typically 20-30oC, varying by species and growth stage. Deviations from this range due to seasonal or climate induced shifts can disrupt enzymatic activity and hormonal signalling, impairing seed imbibition, radicle emergence and root elongation. (Yanjun et al., 2005). Cold soils delay germination and weaken seedling vigour, while excessive warmth accelerates metabolism but impairs root integrity and water balance. Nutrient solubility and uptake is also affected, with phosphorus availability reduced in cooler soils due to limited microbial activity (Blackwell et al., 2010). Microbial processes like decomposition, nitrification and symbiosis are highly temperature sensitive, shaping microbial biomass, diversity and nutrient cycling.
           
    Conservation practices such as mulching, cover cropping and residue management help maintain optimal thermal regimes for microbial health and crop resilience (Lal, 2020). Moreover, soil temperature interacts with moisture dynamics, influencing evapotranspiration, root water uptake and drought tolerance. Recent studies highlight its role in regulating enzymatic activity, membrane fluidity and hormonal signalling, affecting germination, root growth and biomass accumulation  (Yeremko et al., 2025).
           
    Understanding soil temperature dynamics is crucial for optimizing legume productivity, guiding sowing windows, varietal choice and inoculant strategies for climate resilient agriculture. While warmer soils may extend temperate growing seasons but also intensify heat stress and disrupt root–microbe interactions in tropical zones. A nuanced grasp of these dynamics is essential for designing adaptive agronomic practices, selecting thermotolerant cultivars and refining sowing schedules under variable climates.
     
    Root system architecture under soil temperature stress
     
    The rhizosphere is highly sensitive to temperature fluctuations, especially in legumes where root-microbe interactions drive productivity. Soil temperature shapes root system architecture (RSA), influencing elongation, branching and biomass (Luo et al., 2020). RSA governs water and nutrient uptake, microbial colonization and stress resilience. A dual fertilizing layer at the 30/ cm crest buffers soil temperature, enhancing root geometry through shallower angles, lateral proliferation, increased diameter and vertical expansion (Kang et al., 2025). Conversely, cooler root zones (7-13oC) restrict root growth and reduce vascular duct size, impairing mineral uptake and translocation (Miao et al., 2023).
     
    Root elongation
     
    Highly temperature sensitive, elongation in soybean peaks near 30oC, while drops by 70% at 12oC (de Moraes and Gusmao, 2021). Near-zero temperatures halted root extension in cereals like wheat and maize (Morandage et al., 2021), while cooler soils reduce root length density in spring cereals, limiting soil exploration (Qin et al., 2018). Most legumes elongate optimally 20-28oC; below 15oC, cell division slows, while above 35oC root tips are damaged, reducing elongation and lateral root formation.
     
    Lateral root formation
     
    Moderate soil warmth promoting auxin-mediated lateral root development, while excessive heat disrupts hormonal signalling, producing sparse roots. Tripathi et al. (2024) reported that legumes exposed to fluctuating soil temperatures exhibited altered branching patterns and reduced adventitious root density, impairing nodulation and nitrogen fixation.
     
    Biomass accumulation
     
    Root biomass peaks under optimal soil temperature and moisture. Legumes showed higher root biomass cooler temperatures (19-20oC), due to improved water retention and reduced thermal stress (Tchapga et al., 2023). Elevated temperatures accelerate decomposition but reduce biomass via increased respiration and lower carbon allocation. In maize, root dry weight was highest under 30/22oC and 35/27oC regimes (Walne and Reddy, 2022), while warming 4-6oC above ambient deteriorated fine roots and reduce absorptive root biomass (Parts et al., 2019). In cold ecosystems, warming increased root, fungal and fungivore biomass, though bacterial and archaeal levels remained stable (Salazar et al., 2020).
     
    Thermal sensitivity of rhizobial function
     
    Rhizobial activity and colonization under soil temperature stress
     
    Soil temperature is a critical determinant of rhizobial activity, colonization efficiency and legume-rhizobium symbiosis. Rhizobia exhibit optimal metabolic activity and BNF between 20-30oC (Bordeleau and Prévost, 1994), while below 15oC or above 35oC impair bacterial viability, signal exchange and symbiotic function. Low temperatures slow rhizobial metabolism, reduce Nod factor synthesis and delay colonization (Liu et al., 2019). Cold stress also alters gene expression in rhizobia and host roots, affecting early signalling and nodule initiation. In contrast, elevated temperatures may boost root growth but disrupt rhizobial membrane integrity, enzymatic stability and signalling molecule production (Kumar et al., 2023; Caruso et al., 2014).
           
    Soil temperature strongly influences rhizobial motility, chemotaxis and attachment to root hairs, critical steps for colonization. Moderate warmth enhances these processes and boosts nodule biomass, while temperatures outside the optimal (20-30oC) delay colonization (Zhang et al., 2020). Optimal temperatures (20-30oC) favour rhizobial colonization, nodule development and nitrogenase efficiency. Conversely, temperatures below 15oC or above 30oC can hinder nodulation and reduce nitrogen fixation rates (Aranjuelo et al., 2007; Mohammadi et al., 2012). Importantly, rhizobial strains vary in thermal tolerance, with some maintaining symbiotic efficiency under heat stress, making their selection vital for legume cultivation in warming climates  (Asadi Rahmani et al., 2009; Alexandre and Oliveira, 2011).
     
    Rhizobial inoculant formulation and delivery systems
     
    The efficacy of rhizobial inoculants under temperature stress depends on both strain selection and formulation. Carrier-based inoculants using peat, lignite, or charcoal help buffer rhizobia against desiccation and thermal fluctuations, extending shelf life and field viability (Bashan et al., 2014). Liquid inoculants enriched with protective polymers and osmolytes enhance thermal tolerance and rapid colonization, especially in high-temperature environments (Tittabutr et al., 2007). Encapsulation in alginate beads or biochar matrices creates protective microenvironments that moderate temperature and moisture stress  (Schoebitz and López Belchí, 2016). Precision placement of inoculants near the rhizosphere, particularly in mulched or conservation tillage systems, enhances nodulation. Combining thermotolerant strains with optimized formulations and targeted delivery sustains symbiosis under climate variability.
     
    Molecular mechanisms of nodule initiation
     
    Nodule formation begins with molecular dialogue between host roots and compatible rhizobia. Within nodules, rhizobia differentiate into nitrogen-fixing Bacteroides (Ledermann et al., 2021), supported by spatially and temporally regulated signalling networks. Nodules create a microaerobic niche for nutrient exchange and nitrogenase activity. Soil temperature influences nodule development and rhizobial strain competitiveness, for instance, B. diazoefficiens USDA 110/122 perform best at 28/23oC, while B. japonicum USDA 123 prefers cooler conditions (Shiro et al., 2016). Maintaining optimal soil temperatures and using thermotolerant strains with suitable soil management enhances symbiotic efficiency and legume productivity.
     
    Thermal sensitivity of rhizobial function
     
    Soil temperature on nodule formation
     
    Rhizobia form a symbiotic association with legumes, enabling atmospheric nitrogen fixation through nodule formation (Masson-Boivin and Sachs, 2018; Raza et al., 2020). The process begins with root-exuded flavonoids that attract compatible rhizobia and induce Nod factor synthesis (Abd-Alla et al., 2023). These signals recognized by root surface receptors, triggering root hair curling and infection thread formation  (Krönauer and Radutoiu, 2021; Ghantasala and Roy Choudhury, 2022). Soil temperature critically influences rhizobial strain competitiveness and nodule occupancy. For example, B. diazoefficiens USDA 110/122 nodulated optimally at 28/23oC, while B. japonicum USDA 123 prefers cooler conditions, highlighting the importance of temperature-specific strain selection  (Shiro et al., 2016).
     
    Temperature effects on nodule development
     
    Optimal root-zone temperatures for nodule development are species-specific: 25oC for tropical beans, 20oC for peas and 15oC for lentils (Junior et al., 2005). Deviations delay nodule initiation and reduce size, number and growth rate. Rhizobial colonization also varies with temperature, rhizosphere populations rise between 20-30oC, while endophytic movement in chickpea peaks at 25oC (Landa et al., 2004). Co-inoculation with Bradyrhizobium and Azospirillum brasilense enhances nodulation in soybean under 20-30oC, with peak efficiency at 76% soil water retention and 112 nodules per plant (Deak et al., 2019). In contrast, low temperatures (15oC) reduce clover productivity and delay nodulation (Janczarek et al., 2024),  while high temperatures (>40oC) can cause nodulation failure and genetic stress in rhizobia (Hungria and Vargas, 2000).
     
    Role of heat shock proteins in nodule development
     
    In legumes, Heat shock proteins (HSPs) are essential for symbiosis during nodule development, preventing protein aggregation and maintaining cellular homeostasis (Ogden et al., 2017; Flynn et al., 2024). Small HSPs like GmHSP17.9 inhibit thermal aggregation of malate dehydrogenase at 45oC and support early signalling and differentiation  (Yang et al., 2022). HSPs also safeguard nitrogenase enzymes from heat-induced denaturation and oxidative stress, preserving nitrogen fixation (Rajaram and Apte, 2008). Heat-tolerant rhizobial strains such as CIAT899 upregulate specific HSPs (e.g., 21/ kDa) under 40-45oC, enhancing thermotolerance (Michiels et al., 1994). Their stress-induced expression makes HSPs valuable biomarkers and breeding targets for heat-resilient legumes, supporting symbiotic efficiency under climate stress (Aranjuelo et al., 2015).
     
    Cold responsive genes and their impact on nodulation
     
    Cold responsive genes enable legumes to sustain symbiosis under low-temperature stress by encoding proteins such as C-repeat binding factors (CBFs), antifreeze proteins and Osmo protectant enzymes that preserve cellular homeostasis  (Thomashow, 2010). Active rhizobial symbiosis enhances cold tolerance in alfalfa by boosting antioxidant defences and modulating cold-response genes (Liu et al., 2019). Cold stress disrupts hormonal signalling, cytokinin is pivotal for Nod factor transduction and nodule organogenesis (Dolgikh et al., 2016), while low temperatures suppress auxin transporters (PIN1-PIN7), impairing root elongation and gravitropism (Tiwari et al., 2023).  Nitrogenase activity is highly cold-sensitive, declining by 60% in Bradyrhizobium japonicum nodules within 24 hours at 4oC  (Zhang et al., 2014). However, genes like GmFRI-1 help maintain nodulation under cold stress, its overexpression enhances soyabean nodule formation at 4oC, while RNAi silencing inhibits it (Zhang et al., 2025).
     
    Nodule senescence under temperature stress
     
    Root nodule senescence is an orchestrated process involving the programmed death of bacteroids and plant cells, which results in a gradual decline in nitrogen fixation (Tsyganova et al., 2023). Temperature strongly shapes senescence, at 28oC, wild-type SGE nodules senesced centrally after three days, while mutant lines SGEFix”-3 and SGEFix”-7 showed rapid apex and basal senescence within one day  (Serova et al., 2023a). Heat-induced senescence is also governed by hormonal pathways, with upregulation of GA deactivation (PsGA2ox1), ethylene (PsACS2, PsACO1), jasmonic acid (PsLoxN1) and ABA synthesis genes (PsNCED2, PsAO3), alongside downregulation of GA biosynthesis gene PsGA20ox1-collectively promsoting nodule aging (Serova et al., 2023b).
     
    Nitrogen fixation dynamics under soil temperature variability
     
    Biological nitrogen fixation (BNF) is highly soil temperature-sensitive with extremes threaten symbiotic efficiency and crop productivity (Flynn et al., 2024; Kajić et al., 2016). Conservation tillage enhances nodulation and BNF by improving moisture retention, moderating temperature and boosting microbial biomass (Torabian et al., 2019). Root-zone temperature (RZT) is critical, nitrogen fixation in grass pea halts below 10oC, temperate rhizobia peak at 25oC and cold-adapted strains at 15oC (Mahdavi et al., 2010). This highlights the importance of matching rhizobial thermal adaptation to local soil conditions. In Arctic soils, BNF peaks below 14oC with adequate moisture, suggesting vulnerability of cold-adapted diazotrophs to warming (Rousk et al., 2018). In temperate zones, BNF rates rise with temperature, peaking at 35oC under moderate moisture (Li et al., 2018). In chickpea, nitrogenase and nitrate reductase activities peak during flowering but decline at ~39oC, with nitrogenase reductase dropping by 40.12% and nitrogenase by 20.21% (Jain et al., 2014). Ammonium assimilation enzymes GS and GOGAT are even more sensitive to heat stress (Hungria and Kaschuk, 2014). These findings highlight the critical need for temperature resilient symbiotic systems to sustain BNF under climate stress. The interactions between soil temperature and key activities in legume-rhizobium systems are summarized in Table 1 and a graphical abstract (Fig 3).

    Table 1: Optimal soil temperature for the key activities in legume-rhizobium systems.



    Fig 3: Graphical abstract of soil temperature and legume-rhizobium symbiosis.


     
    Agronomic and microbial interventions for soil temperature management
     
    Soil temperature regulates seed germination, root development, microbial activity and nutrient cycling, making its management vital under climate variability. Mulching with straw, leaf litter, or green manures, buffers temperature, conserves moisture and promotes microbial health. In Indian natural farming, mulching synergizes with inputs like Jeevamrit and Bijamrut to enhance nutrient cycling and nitrogen fixation (Lakhani and Bodar, 2025). Mulching also suppresses weeds, reduces evapotranspiration and cold stress, making it especially valuable in dryland and semi-arid regions (Demo and Asefa Bogale, 2024).
           
    Thermotolerant strains of Rhizobium, Azospirillum and phosphate-solubilizing bacteria improve nodulation and nutrient uptake. Inoculants applied with organic carriers and placed near the root zone, often alongside mulching enhance microbial efficacy (Abro et al., 2011). Region-specific formulations are increasingly recommended to match local soils and cropping systems. Sowing window optimization-based on soil temperature thresholds improves germination and seedling vigour. Aligning sowing with seasonal rainfall and temperature patterns boosts yields (Zhang et al., 2019). Longterm Agrometeorological data and crop-weather calendars guide ideal sowing periods for rainfed crops.
           
    Together, these interventions form a low-cost, synergistic framework for climate-resilient agriculture across diverse agro-climatic zones. Integrated with conservation agriculture and ICT-based advisories, they strengthen soil health, microbial diversity and crop productivity under temperature stress.
     
    Way forward
     
    To enhance legume productivity and nitrogen fixation under variable soil temperatures, integrated agronomic management strategies are essential to improve resilience. Advanced inoculant technologies, including encapsulated and polymer-enriched formulations may strengthen the nodulation process. Molecular insights into heat shock proteins, cold-responsive genes and hormonal pathways provide breeding targets. Embedding these approaches in extension programs, policies and farmer training ensures scalable adoption across diverse agro-climatic zones.

    CONCLUSION

    Soil temperature critically shapes root architecture and legume-rhizobium symbiosis, influencing water uptake, nutrient acquisition and nitrogen fixation. Extreme heat or cold impair root development and symbiotic efficiency. Integrating thermotolerant rhizobial strains, optimized inoculants, mulching and conservation tillage helps buffer temperature stress. Strategic sowing windows and root-zone management further enhance nodulation in rainfed systems. Molecular insights into heat shock proteins and cold-responsive genes offer new breeding targets for thermal resilience. Coupled with ICT-based advisories and region-specific agrometeorological data, these interventions can boost legume productivity and soil health. A systems approach, linking genetic, microbial and agronomic innovations is essential for sustaining biological nitrogen fixation and advancing climate-smart agriculture.

    ACKNOWLEDGEMENT

    The authors gratefully acknowledge the Ministry of Social Justice and Empowerment and the University Grants Commission (UGC), Government of India, for the student fellowship and sincerely thank the scientists of the DST–Centre of Excellence on Disaster and Climate Resilient Agriculture, Agro Climate Research Centre, TNAU, Coimbatore, for valuable support in collecting review materials.
     
    Disclaimers
     
    The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect loss resulting from the use of this content.
     
    Informed consent
     
    No animal used during the research.

    CONFLICT OF INTEREST

    The authors declare no conflict of interest.

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