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Symbiotic performance, nitrogen flux and growth of lima bean (Phaseolus lunatus L.) varieties inoculated with different indigenous strains of rhizobia

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Abstract

Legumes, such as lima bean, can form symbiotic relationships with rhizobia and can therefore grow in nitrogen-poor soils. Lima bean varieties in symbiosis with indigenous rhizobia were evaluated for their symbiotic performance over three harvest periods. Four indigenous rhizobial strains (ISOL-16, ISOL-18, ISOL-19 or ISOL-35) were isolated from soil samples in lima bean fields and used separately to inoculate two lima bean varieties (‘boca de moça’ and ‘branca’). Uninoculated, unfertilized plants were used as controls, and uninoculated, nitrogen-supplied plants were used as the nitrogen control. All inoculated plants and the uninoculated control were cultivated using nitrogen-free nutrient solutions in the greenhouse. As expected, the uninoculated plants did not develop nodules on their root systems and were inferior in all evaluated parameters. The lima bean nodulated by Bradyrhizobium exhibited growth variables, nodules parameters, and nitrogen flux values superior to those of plants inoculated with Rhizobium. The highest total chlorophyll values were recorded in lima bean inoculated with Bradyrhizobium, confirming that these plants had the greenest leaves and likely have superior photosynthetic efficiency – a hypothesis supported by the greater growth exhibited by these plants. Nitrogen fixation efficiency was superior in lima bean nodulated by Bradyrhizobium, indicating that this microbe possesses a greater ability to fix nitrogen and provide it continuously to the host plant. The symbiosis between lima bean and Bradyrhizobium sp. ISOL-18 displayed the best values with respect to carbon and nitrogen flow. We conclude that Bradyrhizobium is the most effective at establishing an efficient and successful symbiotic relationship with lima bean and emphasize the potential value of Bradyrhizobium strains as inoculants in lima bean cultivation.

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Acknowledgments

The authors are grateful for the financial support of the National Council of Technological and Scientific Development (CNPq) and the Federal Agency for the Support and Evaluation of Graduate Education (CAPES).

Author information

Authors and Affiliations

  1. Plant Production Post-Graduate Program, Federal University of Piaui, Teresina, PI, Brazil

    Vicente Paulo da Costa Neto & Janaina Barros Siqueira Mendes

  2. Department of Agricultural Engineering and Soil Science, Laboratory of Soil Quality, Federal University of Piaui, Teresina, PI, Brazil

    Ademir Sérgio Ferreira de Araújo

  3. Department of Plant Science, Federal University of Piaui, Teresina, PI, Brazil

    Francisco de Alcântara Neto

  4. Department of Biology, Laboratory of Plant Physiology, Federal University of Piaui, Teresina, PI, Brazil

    Aurenivia Bonifacio

  5. Department of Agricultural Engineering and Soil Science, Laboratory of Soil Microbiology, Federal University of Piaui, CEP, Teresina, PI, 64049-550, Brazil

    Artenisa Cerqueira Rodrigues

Authors
  1. Vicente Paulo da Costa Neto
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  2. Janaina Barros Siqueira Mendes
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  3. Ademir Sérgio Ferreira de Araújo
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  4. Francisco de Alcântara Neto
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  5. Aurenivia Bonifacio
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  6. Artenisa Cerqueira Rodrigues
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Corresponding author

Correspondence to Artenisa Cerqueira Rodrigues.

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Highlights

• Inoculation with Bradyrhizobium strains induces better N-flux and growth in lima bean

• N-fix efficiency was superior in lima bean nodulated by Bradyrhizobium strains

• Bradyrhizobium is most efficient in establishing a successful symbiotic relationship with lima bean

Electronic supplementary material

Supplemental Fig. S1

Stem diameter of ‘boca de moça’ (A) and ‘branca’ (B) lima bean varieties separately inoculated with four indigenous rhizobia, Rhizobium sp. strain ISOL-16 or Bradyrhizobium sp. strain ISOL-18, ISOL-19 or ISOL-35, at flowering, pod setting or pod filling. Uninoculated nitrogen-supplied plants were used as a nitrogen control, while uninoculated plants were used as the absolute control. In each harvest period, different uppercase letters represent significant differences among treatments in each variety whereas different lowercase letters indicate significant differences between the two varieties (boca de moça and branca). All mean comparisons were performed using Tukey’s test (P < 0.05). (DOCX 24 kb)

Supplemental Fig. S2

Root length of ‘boca de moça’ (A) and ‘branca’ (B) lima bean varieties separately inoculated with four indigenous rhizobia, Rhizobium sp. strain ISOL-16 or Bradyrhizobium sp. strain ISOL-18, ISOL-19 or ISOL-35, at flowering, pod setting or pod filling. Uninoculated nitrogen-supplied plants were used as a nitrogen control, while uninoculated plants were used as the absolute control. In each harvest period, different uppercase letters represent significant differences among treatments in each variety whereas different lowercase letters indicate significant differences between the two varieties (boca de moça and branca). All mean comparisons were performed using Tukey’s test (P < 0.05). (DOCX 24 kb)

Supplemental Fig. S3

Nitrogen content of ‘boca de moça’ (A) and ‘branca’ (B) lima bean varieties separately inoculated with four indigenous rhizobia, Rhizobium sp. strain ISOL-16 or Bradyrhizobium sp. strain ISOL-18, ISOL-19 or ISOL-35, at flowering, pod setting or pod filling. Uninoculated nitrogen-supplied plants were used as a nitrogen control, while uninoculated plants were used as the absolute control. In each harvest period, different uppercase letters represent significant differences among treatments in each variety whereas different lowercase letters indicate significant differences between the two varieties (boca de moça and branca). All mean comparisons were performed using Tukey’s test (P < 0.05). (DOCX 23 kb)

Supplemental Fig. S4

Total chlorophyll of ‘boca de moça’ (A) and ‘branca’ (B) lima bean varieties separately inoculated with four indigenous rhizobia, Rhizobium sp. strain ISOL-16 or Bradyrhizobium sp. strain ISOL-18, ISOL-19 or ISOL-35, at flowering, pod setting or pod filling. Uninoculated nitrogen-supplied plants were used as a nitrogen control, while uninoculated plants were used as the absolute control. In each harvest period, different uppercase letters represent significant differences among treatments in each variety whereas different lowercase letters indicate significant differences between the two varieties (boca de moça and branca). FCI = Falker chlorophyll index. All mean comparisons were performed using Tukey’s test (P < 0.05). (DOCX 24 kb)

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da Costa Neto, V.P., Mendes, J.B.S., de Araújo, A.S.F. et al. Symbiotic performance, nitrogen flux and growth of lima bean (Phaseolus lunatus L.) varieties inoculated with different indigenous strains of rhizobia. Symbiosis 73, 117–124 (2017). https://doi.org/10.1007/s13199-017-0475-6

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