Physiology and metabolism of grafted bell pepper in response to low root-zone temperature
Moses Kwame Aidoo
A , Tal Sherman B , Naftali Lazarovitch A , Aaron Fait A and Shimon Rachmilevitch A C
+ Author Affiliations
- Author Affiliations
A French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Israel.
B Zeraim Gedera, Syngenta, Israel.
C Corresponding author. Email: rshimon@bgu.ac.il
Functional Plant Biology 46(4) 339-349 https://doi.org/10.1071/FP18206
Submitted: 8 August 2018 Accepted: 4 December 2018 Published: 15 January 2019
Abstract
Low temperature is a prominent limiting factor for tropical originated crops production in temperate regions, particularly during cool-season production. The diverse response of two rootstocks (Canon-sensitive and S103-tolerant to low root-zone temperature) was studied when exposed to aeroponically different temperature regimes at the root zone: constant low temperature of 14°C low root-zone temperature (LRZT), transient exposure to LRZT of 27–14−27°C and control temperature of 27°C. Gas exchange, shoot dry mass, and root morphology were measured. Shifts in central and secondary metabolite levels in the leaves and roots were examined by gas chromatography-mass spectrometry (GC-MS). Low root-zone temperature inhibited photosynthesis and transpiration of both grafted bell pepper plants; however, self-grafted Canon physiology was impeded to a greater extent compared with Canon grafted onto rootstock S103. Rootstock S103 demonstrated higher sink potential contributing to milder reduction of photosynthesis and transpiration during stress compared with self-grafted Canon. This reduction of gas exchange led to a significant reduction of root maximum length and root dry mass in self-grafted Canon in response to the stress at 14°C compared with Canon grafted onto rootstock S103. In response to stress, GC-MS metabolite profiling showed enhance metabolism in both cultivars’ leaves, as well as in the roots irrespective of the developmental stage of the plant. This evidence combined indicates enhance gas exchange and carbon assimilation when bell pepper is grafted on S103 under low root-zone temperature.
Additional keywords: aeroponic, central metabolism, photosynthesis, secondary metabolism, stress, transpiration.
References
Aidoo MK, Bdolach E, Fait A, Lazarovitch N, Rachmilevitch S (2016) Tolerance to high soil temperature in foxtail millet (Setaria italica L.) is related to shoot and root growth and metabolism. Plant Physiology and Biochemistry 106, 73–81.| Tolerance to high soil temperature in foxtail millet (Setaria italica L.) is related to shoot and root growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 27149034PubMed |
Aidoo MK, Sherman T, Lazarovitch N, Fait A, Rachmilevitch S (2017) A bell pepper cultivar tolerant to chilling enhanced nitrogen allocation and stress related metabolite accumulation in the roots in response to low root zone temperature. Physiologia Plantarum 161, 196–210.
| A bell pepper cultivar tolerant to chilling enhanced nitrogen allocation and stress related metabolite accumulation in the roots in response to low root zone temperature.Crossref | GoogleScholarGoogle Scholar | 28444904PubMed |
Aidoo MK, Sherman T, Ephrath JE, Fait A, Rachmilevitch S, Lazarovitch N (2018) Grafting as a method to increase the tolerance response of bell pepper to extreme temperatures. Vadose Zone Journal 17, 170006
| Grafting as a method to increase the tolerance response of bell pepper to extreme temperatures.Crossref | GoogleScholarGoogle Scholar |
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
| Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 18662937PubMed |
Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 101, 15243–15248.
| A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15383661PubMed |
Du H, Wanga Z, Yub W, Liub Y, Huang B (2011) Differential metabolic responses of perennial grass Cynodon transvaalensis × Cynodon dactylon (C4) and Poa Pratensis (C3) to heat stress. Physiologia Plantarum 141, 251–264.
| Differential metabolic responses of perennial grass Cynodon transvaalensis × Cynodon dactylon (C4) and Poa Pratensis (C3) to heat stress.Crossref | GoogleScholarGoogle Scholar | 21114672PubMed |
Engels C (1994) Root and shoot meristem temperature on shoot to root dry matter partitioning and the internal concentrations of nitrogen and carbohydrates in maize and wheat. Annals of Botany 73, 211–219.
| Root and shoot meristem temperature on shoot to root dry matter partitioning and the internal concentrations of nitrogen and carbohydrates in maize and wheat.Crossref | GoogleScholarGoogle Scholar |
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 14–19.
| Highway or byway: the metabolic role of the GABA shunt in plants.Crossref | GoogleScholarGoogle Scholar | 18155636PubMed |
Griffith M, Yaish MWF (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends in Plant Science 9, 399–405.
| Antifreeze proteins in overwintering plants: a tale of two activities.Crossref | GoogleScholarGoogle Scholar | 15358271PubMed |
Guy C, Kaplana F, Kopkac J, Selbigc J, Hinchac DK (2008) Metabolomics of temperature stress. Physiologia Plantarum 132, 220–235.
He J, Qin L, Lee SK (2013) Root-zone CO2 and root-zone temperature effects on photosynthesis and nitrogen metabolism of aeroponically grown lettuce (Lactuca sativa L.) in the tropics. Photosynthetica 51, 330–340.
| Root-zone CO2 and root-zone temperature effects on photosynthesis and nitrogen metabolism of aeroponically grown lettuce (Lactuca sativa L.) in the tropics.Crossref | GoogleScholarGoogle Scholar |
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experimental Station Circular 347. Riverside, CA, USA.
Hochberg U, Batushansk A, Degu A, Rachmilevitch S, Fait A (2015) Metabolic and physiological responses of Shiraz and Cabernet Sauvignon (Vitis vinifera L.) to elevated temperatures. International Journal of Molecular Sciences 16, 24276–24294.
| Metabolic and physiological responses of Shiraz and Cabernet Sauvignon (Vitis vinifera L.) to elevated temperatures.Crossref | GoogleScholarGoogle Scholar | 26473851PubMed |
Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends in Ecology & Evolution 15, 56–61.
| Biological consequences of global warming: is the signal already apparent?Crossref | GoogleScholarGoogle Scholar |
Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310–316.
| Complexity of the heat stress response in plants.Crossref | GoogleScholarGoogle Scholar | 17482504PubMed |
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387–396.
| Gas chromatography mass spectrometry-based metabolite profiling in plants.Crossref | GoogleScholarGoogle Scholar | 17406261PubMed |
López-Marín J, González A, Pérez-Alfocea F, Egea-Gilabert C, Fernández JA (2013) Grafting is an efficient alternative to shading screens to alleviate thermal stress in greenhouse-grown sweet pepper. Scientia Horticulturae 149, 39–46.
| Grafting is an efficient alternative to shading screens to alleviate thermal stress in greenhouse-grown sweet pepper.Crossref | GoogleScholarGoogle Scholar |
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics 444, 139–158.
| Cold, salinity and drought stresses: an overview.Crossref | GoogleScholarGoogle Scholar | 16309626PubMed |
Mercado JA, Trigo MM, Reid MS, Valpuesta V, Quesada MA (1997) Effects of low temperature on pepper pollen morphology and fertility: evidence of cold induced exine alterations. Journal of Horticultural Science 72, 317–326.
| Effects of low temperature on pepper pollen morphology and fertility: evidence of cold induced exine alterations.Crossref | GoogleScholarGoogle Scholar |
Ntatsi G, Savvas D, Klaering HP, Schwarz D (2014) Growth, yield, and metabolic responses of temperature-stressed tomato to grafting onto rootstocks differing in cold tolerance. Journal of Horticultural Science 139, 230–243.
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? Journal of Experimental Botany 62, 869–882.
| Photosynthesis and drought: can we make metabolic connections from available data?Crossref | GoogleScholarGoogle Scholar | 21172816PubMed |
Rachmilevitch S, Lambers H, Huang B (2008) Short-term and long-term root respiratory acclimation to elevated temperatures associated with root thermotolerance for two agrostis grass species. Journal of Experimental Botany 59, 3803–3809.
| Short-term and long-term root respiratory acclimation to elevated temperatures associated with root thermotolerance for two agrostis grass species.Crossref | GoogleScholarGoogle Scholar | 18977747PubMed |
Rewald B, Meinen C, Trockenbrodt M, Ephrath JE, Rachmilevitch S (2012) Root taxa identification in plant mixtures – current techniques and future challenges. Plant and Soil 359, 165–182.
| Root taxa identification in plant mixtures – current techniques and future challenges.Crossref | GoogleScholarGoogle Scholar |
Ristic Z, Ashworth EN (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation. Protoplasma 172, 111–123.
| Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation.Crossref | GoogleScholarGoogle Scholar |
Roessner U, Willmitzer L, Fernie AR (2001) High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiology 127, 749–764.
| High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies.Crossref | GoogleScholarGoogle Scholar | 11706160PubMed |
Saeed AI, Hagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li JW, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods in Enzymology 411, 134–193.
| TM4 microarray software suite.Crossref | GoogleScholarGoogle Scholar | 16939790PubMed |
Savvas D, Colla G, Rouphael Y, Schwarz D (2010) Amelioration of heavy metal and nutrient stress in fruit vegetables by grafting. Scientia Horticulturae 127, 156–161.
| Amelioration of heavy metal and nutrient stress in fruit vegetables by grafting.Crossref | GoogleScholarGoogle Scholar |
Schwarz D, Rouphael Y, Colla G, Venema JH (2010) Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Scientia Horticulturae 127, 162–171.
| Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants.Crossref | GoogleScholarGoogle Scholar |
Setter TL, Greenway H (1988) Growth reductions of rice at low root temperature: decreases in nutrient uptake and development of chlorosis. Journal of Experimental Botany 39, 811–829.
| Growth reductions of rice at low root temperature: decreases in nutrient uptake and development of chlorosis.Crossref | GoogleScholarGoogle Scholar |
Shelef O, Lazarovitch N, Rewald B, Golan-Goldhirsh A, Rachmilevitch S (2010) Root halotropism? Salinity effects on Bassia indica roots. Plant Biosystems 144, 471–478.
| Root halotropism? Salinity effects on Bassia indica roots.Crossref | GoogleScholarGoogle Scholar |
Venema JH, Linger P, van Heusden AW, van Hasselt PR, Brüggemann W (2005) The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biology 7, 118–130.
| The inheritance of chilling tolerance in tomato (Lycopersicon spp.).Crossref | GoogleScholarGoogle Scholar | 15822007PubMed |
Venema JH, Dijk BE, Bax JM, van Hasselt PR, Elzenga JTM (2008) Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance. Environmental and Experimental Botany 63, 359–367.
| Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance.Crossref | GoogleScholarGoogle Scholar |
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society B, Biological Sciences 272, 2561–2569.
| Shifts in phenology due to global climate change: the need for a yardstick.Crossref | GoogleScholarGoogle Scholar | 16321776PubMed |
Wang X Zhang W Miao Y Gao L 2016
Wu W, Cheng S (2014) Root genetic research, an opportunity and challenge to rice improvement. Field Crops Research 165, 111–124.
| Root genetic research, an opportunity and challenge to rice improvement.Crossref | GoogleScholarGoogle Scholar |
Xu C, Huang B (2008) Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance. Journal of Experimental Botany 59, 4183–4194.
| Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance.Crossref | GoogleScholarGoogle Scholar | 19008411PubMed |
Yan QY, Duan ZQ, Mao JD, Li X, Dong F (2013) Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response. Journal of Integrative Agriculture 12, 1450–1460.
| Low root zone temperature limits nutrient effects on cucumber seedling growth and induces adversity physiological response.Crossref | GoogleScholarGoogle Scholar |
Zheng N, Wang ML, Wang HT, Ai XZ (2009) Effects of grafting on photosynthesis of sweet pepper seedlings under low temperature and weak light intensity. Ying Yong Sheng Tai Xue Bao 20, 591–596.
Zhou YH, Wu JX, Zhu LJ, Shi K, Yu JQ (2009) Effects of phosphorus and chilling under low irradiance on photosynthesis and growth of tomato plants. Biologia Plantarum 53, 378–382.
| Effects of phosphorus and chilling under low irradiance on photosynthesis and growth of tomato plants.Crossref | GoogleScholarGoogle Scholar |
