Sensitivity of leaflet growth rate to drought predicts yield in common bean (Phaseolus vulgaris)
Amber N. Hageman
A , Milan O. Urban B and Elizabeth Van Volkenburgh A C
+ Author Affiliations
- Author Affiliations
A University of Washington, Life Sciences Building, W Stevens Way NE, Seattle, WA 98195, USA.
B Bioversity International and the International Center for Tropical Agriculture (CIAT), Km 17 Recta Cali-Palmira CP 763537, Apartado Aereo 6713, Cali, Colombia.
C Corresponding author. Email: lizvanv@uw.edu
Functional Plant Biology 47(9) 792-802 https://doi.org/10.1071/FP19332
Submitted: 19 November 2019 Accepted: 29 March 2020 Published: 19 June 2020
Abstract
Although drought limits yield by decreasing photosynthesis and therefore biomass accumulation, biomass is not the strongest predictor of yield under drought in common beans (Phaseolus vulgaris L.). Instead, resource partitioning from pod walls into seeds is a stronger correlate. Our aim was to determine whether growth rates of developing leaflets and pods, as independent indicators of sink strength, predict resource partitioning into seeds. Using 20 field-grown genotypes, we paired biomass, yield, and resource partitioning data with leaflet and pod growth rates under well-watered and droughted conditions. We hypothesised that genotypes with faster growing leaflets and pods under drought would fill seeds better. However, we found that leaflet and pod growth rates did not predict partitioning to seeds; rather, sensitivity of leaflet growth rate to drought was a good predictor of yield reduction. Further, plants with rapidly growing leaves under well-watered conditions were most vulnerable to decreases in leaflet growth rate under drought. This suggests that lines that inherited a conservative growth strategy were better able to maintain yield by allocating resources to seeds. Our findings indicate that inherent sensitivity of leaflet growth rate to drought may be used as a predictor of partitioning and yield in common beans.
Additional keywords: allocation, drought resistance, legumes, pod harvest index, sink strength.
References
Andrade ER, Ribeiro VN, Azevedo CVG, Chiorato AF, Williams TCR, Carbonell SAM (2016) Biochemical indicators of drought tolerance in the common bean (Phaseolus vulgaris L.). Euphytica 210, 277–289.| Biochemical indicators of drought tolerance in the common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Assefa T, Beebe SE, Rao IM, Cuasquer JB, Duque MC, Rivera M, Battisti A, Lucchin M (2013) Pod harvest index as a selection criterion to improve drought resistance in white pea bean. Field Crops Research 148, 24–33.
| Pod harvest index as a selection criterion to improve drought resistance in white pea bean.Crossref | GoogleScholarGoogle Scholar |
Banan D, Van Volkenburgh E (2012) Growth response of common bean (Phaseolus vulgaris L.) lines to water deficit. Bean Improvement Cooperative Annual Reports 55, 1–2.
Beebe SE, Rao IM, Cajiao C, Grajales M (2008) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Science 48, 582–592.
| Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments.Crossref | GoogleScholarGoogle Scholar |
Beebe SE, Rao IM, Blair MW, Acosta-Gallegos JA (2013) Phenotyping common beans for adaptation to drought. Frontiers in Physiology 4, 35
| Phenotyping common beans for adaptation to drought.Crossref | GoogleScholarGoogle Scholar | 23507928PubMed |
Blum DE, Elzenga JTM, Linnemeyer PA, Van Volkenburgh E (1992) Stimulation of growth and ion uptake in bean leaves by red and blue light. Plant Physiology 100, 1968–1975.
| Stimulation of growth and ion uptake in bean leaves by red and blue light.Crossref | GoogleScholarGoogle Scholar | 16653225PubMed |
Cuellar-Ortiz SM, De La Paz Arrieta-Montiel M, Acosta-Gallegos J, Covarrubias AA (2008) Relationship between carbohydrate partitioning and drought resistance in common bean. Plant, Cell & Environment 31, 1399–1409.
| Relationship between carbohydrate partitioning and drought resistance in common bean.Crossref | GoogleScholarGoogle Scholar |
Davies WJ, Van Volkenburgh E (1983) The influence of water deficit on the factors controlling the daily pattern of growth of Phaseolus trifoliates. Journal of Experimental Botany 34, 987–999.
Diaz LM, Ricaurte J, Tovar E, Cajiao C, Terán H, Grajales M, Polanía J, Rao I, Beebe S, Raatz B (2018) QTL analyses for tolerance to abiotic stresses in a common bean (Phaseolus vulgaris L.) population. PLoS One 13, e0202342
| QTL analyses for tolerance to abiotic stresses in a common bean (Phaseolus vulgaris L.) population.Crossref | GoogleScholarGoogle Scholar | 30543633PubMed |
Feller C, Bleiholder H, Buhr L, Hack H, Hess M, Klose R, Meier U, Stauss R, van den Boom T, Weber E (1995) Phänologische Entwicklungsstadien von Gemüsepflanzen: II. Fruchtgemüse und Hülsenfrüchte. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 47, 217–232.
Hageman A, Urban MO, Van Volkenburgh E (2019) Drought sensitivity of leaflet growth, biomass accumulation, and resource partitioning predicts yield in common bean. bioRxiv.
| Drought sensitivity of leaflet growth, biomass accumulation, and resource partitioning predicts yield in common bean.Crossref | GoogleScholarGoogle Scholar |
Khush GS (1999) Green revolution: preparing for the 21st century. Genome 42, 646–655.
| Green revolution: preparing for the 21st century.Crossref | GoogleScholarGoogle Scholar | 10464789PubMed |
Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62, 1715–1729.
| Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs.Crossref | GoogleScholarGoogle Scholar | 21239376PubMed |
Omae H, Kumar A, Shono M (2012) Adaptation to high temperature and water deficit in the common bean (Phaseolus vulgaris L.) during the reproductive period. Le Journal de Botanique 2012, 803413
| Adaptation to high temperature and water deficit in the common bean (Phaseolus vulgaris L.) during the reproductive period.Crossref | GoogleScholarGoogle Scholar |
Polania J, Rao IM, Cajiao C, Rivera M, Raatz B, Beebe S (2016) Physiological traits associated with drought resistance in Andean and Mesoamerican genotypes of common bean (Phaseolus vulgaris L.). Euphytica 210, 17–29.
| Physiological traits associated with drought resistance in Andean and Mesoamerican genotypes of common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Polania J, Rao IM, Caijao C, Grajales M, Rivera M, Valasquez F, Raatz B, Beebe SE (2017) Shoot and root traits contribute to drought resistance in recombinant inbred lines of MD 23–24 × SEA 5 of common bean. Frontiers in Plant Science 8, 29–6.
| Shoot and root traits contribute to drought resistance in recombinant inbred lines of MD 23–24 × SEA 5 of common bean.Crossref | GoogleScholarGoogle Scholar |
Rao IM, Beebe SE, Polania J, Grajales M, Cajiao C, Ricaurte J, Garcia R, Rivera M (2017) Evidence for genotypic differences among elite lines of common bean in the ability to remobilize photosynthate to increase yield under drought. The Journal of Agricultural Science 155, 857–875.
| Evidence for genotypic differences among elite lines of common bean in the ability to remobilize photosynthate to increase yield under drought.Crossref | GoogleScholarGoogle Scholar |
Rosales MA, Ocampo E, Rodríguez-Valentín R, Olvera-Carrillo Y, Acosta-Gallegos J, Covarrubias AA (2012) Plant physiology and biochemistry physiological analysis of common bean (Phaseolus vulgaris L.) cultivars uncovers characteristics related to terminal drought resistance. Plant Physiology and Biochemistry 56, 24–34.
| Plant physiology and biochemistry physiological analysis of common bean (Phaseolus vulgaris L.) cultivars uncovers characteristics related to terminal drought resistance.Crossref | GoogleScholarGoogle Scholar | 22579941PubMed |
Shibles RM, Weber CR (1966) Interception of solar radiation and dry matter production by various soybean planting patterns. Crop Science 6, 55–59.
| Interception of solar radiation and dry matter production by various soybean planting patterns.Crossref | GoogleScholarGoogle Scholar |
Smith MR (2018) Novel techniques to improve yield quantity and quality in common bean. PhD thesis. Faculty of Agriculture and Environment, The University of Sydney, Sydney, NSW, Australia. Available at https://ses.library.usyd.edu.au/handle/2123/17952?mode=full [Verified 22 May 2020]
Smith MR, Veneklaas E, Polania J, Rao IM, Beebe SE, Merchant A (2019) Field drought conditions impact yield but not nutritional quality of the seed in common bean (Phaseolus vulgaris L.). PLoS One 14, e0217099
| Field drought conditions impact yield but not nutritional quality of the seed in common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 31170187PubMed |
Tegeder M, Thomas M, Hetherington L, Wang X-D, Offler CE, Patrick JW (2000) Genotypic differences in seed growth rates of Phaseolus vulgaris L. II. Factors contributing to cotyledon sink activity and sink size. Australian Journal of Plant Physiology 27, 119–128.
| Genotypic differences in seed growth rates of Phaseolus vulgaris L. II. Factors contributing to cotyledon sink activity and sink size.Crossref | GoogleScholarGoogle Scholar |
Thung M, Rao IM (1999) Integrated management of abiotic stresses. In ‘Common bean improvement in the twenty-first century’. (Ed. SP Singh) pp. 331–370. (Kluwer Academic Publications: Dordrecht, Netherlands)
Van Volkenburgh E (1999) Leaf expansion – an integrating plant behaviour. Plant, Cell & Environment 22, 1463–1473.
| Leaf expansion – an integrating plant behaviour.Crossref | GoogleScholarGoogle Scholar |
Van Volkenburgh E, Cleland RE (1980) Proton excretion and cell expansion in bean leaves. Planta 148, 273–278.
| Proton excretion and cell expansion in bean leaves.Crossref | GoogleScholarGoogle Scholar | 24309830PubMed |
Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytologist 116, 341–381.
| The control of carbon partitioning in plants.Crossref | GoogleScholarGoogle Scholar |
Watson DJ 1952) The Physiological Basis of Variation in Yield. pp. 101–145.
Westgate ME, Grant DT (1989) Effect of water deficits on seed development in soybean I. Tissue water status. Plant Physiology 91, 975–979.
| Effect of water deficits on seed development in soybean I. Tissue water status.Crossref | GoogleScholarGoogle Scholar | 16667164PubMed |
