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Plant density effects on quinoa yield, leaf anatomy, ultrastructure and gas exchange

Published online by Cambridge University Press:  25 August 2022

J. A. González Open the ORCID record for J. A. González [Opens in a new window] ,
M. I. Mercado Open the ORCID record for M. I. Mercado [Opens in a new window] ,
L. Martinez-Calsina ,
L. E. Erazzú ,
S. E. Buedo ,
D. A. González  and
G. I. Ponessa
J. A. González
Affiliation:
Instituto de Ecología, Comportamiento y Conservación, Fundación Miguel Lillo, Miguel Lillo 251, Tucumán, Argentina
M. I. Mercado*
Affiliation:
Instituto de Morfología Vegetal, Fundación Miguel Lillo, Miguel Lillo 251, Tucumán, Argentina
L. Martinez-Calsina
Affiliation:
Famaillá, Instituto Nacional de Tecnología Agropecuaria (INTA), Tucumán, Argentina Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Tucumán, Argentina
L. E. Erazzú
Affiliation:
Famaillá, Instituto Nacional de Tecnología Agropecuaria (INTA), Tucumán, Argentina Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Tucumán, Argentina
S. E. Buedo
Affiliation:
Instituto de Ecología, Comportamiento y Conservación, Fundación Miguel Lillo, Miguel Lillo 251, Tucumán, Argentina
D. A. González
Affiliation:
Instituto de Bioprospección y Fisiología Vegetal (INBIOFIV), CONICET-UNT; Facultad de Ciencias Naturales e Instituto Miguel Lillo, Tucumán, Argentina
G. I. Ponessa
Affiliation:
Instituto de Morfología Vegetal, Fundación Miguel Lillo, Miguel Lillo 251, Tucumán, Argentina
*
Author for correspondence: M. I. Mercado, E-mail: mimercado@lillo.org.ar
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Abstract

To study the impact of plant density on Chenopodium quinoa (c.v. CICA-17) achene yield and its relationship with morphology, leaf anatomy and gas exchange in the absence of water stress, field trials were conducted at 1995 m asl in Northwestern Argentina. Two plant densities were evaluated; low density (LD) 7.2 plants/m (120 240 pl/ha) and high density (HD) 27.9 plants/m (465 930 pl/ha). HD treatment caused light competition, inducing morphological and anatomical changes in Quinoa plants. Plants grown under HD conditions showed decreases in plant height and stem diameter, lower stomatal dimensions and densities, and thinner leaf blades. Compensation strategies such as increases in specific leaf area and a higher number chloroplasts per palisade cell were observed, nevertheless these changes did not fully compensate C absorption and gas exchange limitations, therefore limiting the uptake of N and P and resulting in a 53.2% lower yield of HD compared to LD. Considering the ability of quinoa plants to change its morphology and anatomy, further studies with intermediate plant densities are necessary in order to determine if it is possible to achieve higher yields and to increase the efficiency in the use of the resources.

Keywords

Argentinachloroplastleaf anatomylight competitionphotosynthesis
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 160 , Issue 5 , October 2022 , pp. 349 - 359
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abdalla, D, Jorge, A-B, Abdou, G, Amidou, G, Louis, N and Jacob, S (2020) Effect of different planting techniques and sowing density rates on the development of quinoa. African Journal of Agricultural Research 16, 1325–1333.CrossRefGoogle Scholar
Alandia, G, Rodriguez, JP, Jacobsen, SE, Bazile, D and Condori, B (2020) Global expansion of quinoa and challenges for the Andean region. Global Food Security 26, 100429.CrossRefGoogle Scholar
Andreotti, F, Bazile, D, Biaggi, MC, Callo-Concha, D, Jacquet, J, Jemal, OM, King, OI, Mbosso, C, Padulosi, S, Speelman, EN and Van Noordwijk, M (2022) When neglected species gain global interest: lessons learned from quinoa's boom and bust for teff and minor millet. Global Food Security 32, 100613. https://doi.org/10.1016/j.gfs.2022.100613.CrossRefGoogle Scholar
Angeli, V, Miguel Silva, P, Crispim Massuela, D, Khan, MW, Hamar, A, Khajehei, F, Graeff-Hönninger, S and Piatti, C (2020) quinoa (Chenopodium quinoa Willd.): an overview of the potentials of the ‘golden grain’ and socio-economic and environmental aspects of its cultivation and marketization. Foods 9, 216.CrossRefGoogle ScholarPubMed
Asher, A, Galili, S, Whitney, T and Rubinovich, L (2020) The potential of quinoa (Chenopodium quinoa) cultivation in Israel as a dual-purpose crop for grain production and livestock feed. Scientia Horticulturae 272, 109534.CrossRefGoogle Scholar
Bauer, P, Elbaum, R and Weiss, IM (2011) Calcium and silicon mineralization in land plants: transport, structure and function. Plant Science 180, 746–756.CrossRefGoogle ScholarPubMed
Bazile, D, Bertero, HD and Nieto, C (2015) State of the Art Report on Quinoa Around the World in 2013. Santiago du Chili: FAO, CIRAD, 603 p. http://www.fao.org/quinoa-2013/publications/detail/en/item/278923/icode/?no_mobile=1.Google Scholar
Bazile, D, Jacobsen, S-E and Verniau, A (2016 a) The global expansion of quinoa: trends and limits. Frontiers in Plant Science 7, 622.CrossRefGoogle ScholarPubMed
Bazile, D, Pulvento, C, Verniau, A, Al-Nusairi, M, Ba, D, Breidy, J, Hassan, L, Maarouf, IM, Mambetov, O, Otambekova, M, Sephavand, NA, Shams, A, Souici, D, Miri, K and Padulosi, S (2016 b) Worldwide evaluations of quinoa: preliminary results from post international year of quinoa FAO projects in nine countries. Frontiers in Plant Science 7, 850.CrossRefGoogle ScholarPubMed
Bose, J, Munns, R, Shabala, S, Gilliham, M, Pogson, B and Tyerman, SD (2017) Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. Journal of Experimental Botany 68, 3129–3143.CrossRefGoogle ScholarPubMed
Brodersen, CR, Vogelmann, TC, Williams, WE and Gorton, HL (2007) A new paradigm in leaf-level photosynthesis: direct and diffuse lights are not equal. Plant Cell and Environment 31, 159–164.Google Scholar
Chappelle, EW, Kim, MS and McMurtrey, JE (1992) Ratio analysis of reflectance spectra (RARS): an algorithm for the remote estimation of the concentrations of chlorophyll A, chlorophyll B, and carotenoids in soybean leaves. Remote Sensing of Environment 39, 239–247.CrossRefGoogle Scholar
Croft, H, Chen, JM, Luo, X, Bartlett, P, Chen, B and Staebler, RM (2017) Leaf chlorophyll content as a proxy for leaf photosynthetic capacity. Global Change Biology 23, 3513–3524.CrossRefGoogle ScholarPubMed
Cruz Díaz, I, Chaparro, HN, Díaz, LI and Romero Guerrero, GA (2021) Effect of sowing density on the agronomic performance of quinoa Nariño cultivar and the transmissivity of photosynthetically active radiation in the high tropics of Colombia. Revista Facultad Nacional de Agronomía Medellín 74, 9491–9497.CrossRefGoogle Scholar
Delatorre-Herrera, J, Ruiz, KB and Pinto, M (2021) The importance of non-diffusional factors in determining photosynthesis of two contrasting quinoa ecotypes (Chenopodium quinoa Willd.) subjected to salinity conditions. Plants 10, 927.CrossRefGoogle ScholarPubMed
DeLucía, EH, Nelson, K, Vogelmann, TC and Smith, WK (1996) Contribution of intercellular reflectance to photosynthesis in shade leaves. Plant Cell and Environment 19, 159–170.CrossRefGoogle Scholar
Dizeo de Strittmatter, CD (1973) Nueva técnica de diafanización. Boletín de la Sociedad Argentina de Botánica 1, 126–129. https://botanicaargentina.org.ar/wp-content/uploads/2018/09/126-129013.pdf.Google Scholar
Eisa, SE, El-Samad, EH, Hussin, SA, Ali, EA, Ebrahim, M, González, JA, Ordano, M, Erazzú, LE, El-Bordeny, NE and Abdel-Ati, AA (2018) Quinoa in Egypt – plant density effects on seed yield and nutritional quality in marginal regions. Middle East Journal of Applied Sciences 8, 515–522. https://www.curresweb.com/mejas/mejas/2018/515-522.pdf.Google Scholar
El Hazzam, K, Hafsa, J, Sobeh, M, Mhada, M, Taourirte, M, EL Kacimi, K and Yasri, A (2020) An insight into saponins from quinoa (Chenopodium quinoa Willd): a review. Molecules 25, 1059.CrossRefGoogle ScholarPubMed
Eustis, A, Murphy, KM and Barrios-Masias, FH (2020) Leaf gas exchange performance of ten Quinoa genotypes under a simulated heat wave. Plants 9, 81.CrossRefGoogle Scholar
Evans, JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.CrossRefGoogle Scholar
Evans, JR and Poorter, H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment 24, 755–767.CrossRefGoogle Scholar
Evans, JR and Vogelmann, TC (2003) Profiles of 14 C fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant Cell and Environment 26, 547–560.CrossRefGoogle Scholar
Evans, J, Caemmerer, S, Setchell, B and Hudson, G (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of RuBisCo. Functional Plant Biology 21, 475–495.CrossRefGoogle Scholar
Feng, Y, Lingyang, F, Qinlin, L, Xiaoling, W, Yuanfang, F, Muhammad, AR, Yajiao, C, Junxu, C, Xiaochun, W, Taiwen, Y, Weiguo, L, Jiang, L, Junbo, D, Kai, S and Wenyu, Y (2018) Effect of interactions between light intensity and red-to-far-red ratio on the photosynthesis of soybean leaves under shade condition. Environmental and Experimental Botany 150, 79–87.Google Scholar
Franklin, KA and Whitelam, GC (2004) Light signals, phytochromes and cross-talk with other environmental cues. Journal of Experimental Botany 55, 271–276.CrossRefGoogle ScholarPubMed
Fuentes, F, Bazile, D, Bhargava, A and Martinez, EA (2012) Implications of farmers’ seed exchanges for on-farm conservation of quinoa, as revealed by its genetic diversity in Chile. Journal of Agricultural Science 150, 702–716.CrossRefGoogle Scholar
Garnier, E, Cordonnier, P, Guillerm, J-L and Sonié, L (1997) Specific leaf area and leaf nitrogen concentration in annual and perennial grass species growing in Mediterranean old-fields. Oecologia 111, 490–498.CrossRefGoogle ScholarPubMed
Geissler, N, Hussin, S, El-Far, MMM and Koyro, H-W (2015) Elevated atmospheric CO2 concentration leads to different salt resistance mechanisms in a C3 (Chenopodium quinoa) and a C4 (Atriplex nummularia) halophyte. Environmental and Experimental Botany 118, 67–77.CrossRefGoogle Scholar
González, JA, Bruno, M, Valoy, M and Prado, FE (2011) Genotypic variation of gas exchange parameters and leaf stable carbon and nitrogen isotopes in ten quinoa cultivars grown under drought. Journal of Agronomy and Crop Science 197, 81–93.CrossRefGoogle Scholar
González, JA, Ponessa, GI, Buedo, SE, Mercado, MI and Prado, FE (2014) Asimilación fotosintética máxima en variedades de quinoa (Chenopodium quinoa) de diferentes orígenes geográficos y su relación con la morfología foliar. Lilloa 51, 177–193. http://www.lillo.org.ar/revis/lilloa/2014-51-2/06.pdf.Google Scholar
González, JA, Eisa, S, Hussin, S and Prado, FE (2015) Quinoa: an Incan crop to face global changes in agriculture. In Murphy, KS and Matanguihan, J (eds). Quinoa: Improvement and Sustainable Production. New Jersey, U.S: John Wiley & Sons, Inc. pp. 1–18.Google Scholar
González, JA, Martín, GO, Bruno, MA and Prado, FE (2016) La ‘quínoa’ (Chenopodium quinoa) como alternativa forrajera en la zona de los Valles Calchaquíes (Noroeste Argentino). Lilloa 53, 74–81. http://www.lillo.org.ar/journals/index.php/lilloa/article/view/123.Google Scholar
González, JA, Jacobsen, SE, Buedo, SE, Erazzú, LE, González, DA and Prado, FE (2019) Evaluation of photosynthetic capacity and grain yield of the sea level quinoa variety Titicaca grown in a highland region of Northwest Argentine. Middle East Journal of Applied Sciences 09, 888–900.Google Scholar
He, H, Veneklaas, EJ, Kuo, J and Lambers, H (2014) Physiological and ecological significance of biomineralization in plants. Trends in Plant Science 19, 166–174.CrossRefGoogle ScholarPubMed
Heitholt, J and Sassenrath-Cole, G (2010) Inter-plant competition: growth responses to plant density and row spacing. In Stewart, JM, Oosterhuis, DM, Heitholt, JJ and Mauney, JR (eds). Physiology of Cotton. Dordrecht: Springer, pp. 179–186. https://doi.org/10.1007/978-90-481-3195-2_17.CrossRefGoogle Scholar
Hendry, GAF and Price, AH (1993) Stress indicators: chlorophylls and carotenoids. In Hendry, GAF and Grime, JP (eds). Methods in Comparative Plant Ecology. London, Chapman Hall, pp. 148–152.CrossRefGoogle Scholar
Hinojosa, L, Leguizamo, A, Carpio, C, Muñoz, D, Mestanza, C, Ochoa, J, Castillo, C, Murillo, A, Villacréz, E, Monar, C, Pichazaca, N and Murphy, K (2021) Quinoa in Ecuador: recent advances under global expansion. Plants 10, 298.CrossRefGoogle ScholarPubMed
Hodgson, GL and Blackman, GE (1957) An analysis of the influence of plant density on the growth of Vicia faba: II. The significance of competition for light in relation to plant development at different densities. Journal of Experimental Botany 8, 195–219.CrossRefGoogle Scholar
Horner, HT, Wanke, S, Oelschlägel, B and Samain, M-S (2017) Peruvian window-leaved Peperomia taxa display unique crystal macropatterns in high-altitude environments. International Journal of Plant Sciences 178, 157–167.CrossRefGoogle Scholar
Jacobsen, S-E (2015) Adaptation and scope for quinoa in northern latitudes of Europe. In Bazile, D, Bertero, HD and Nieto, C (eds). State of the Art Report on Quinoa Around the World in 2013. Rome: FAO, pp. 436–446.Google Scholar
Jacobsen, S-E and Christiansen, JL (2016) Some agronomic strategies for organic quinoa (Chenopodium quinoa Willd.). Journal of Agronomy and Crop Science 202, 454–463.CrossRefGoogle Scholar
Jacobsen, S-E, Jørgensen, I and Stølen, O (1994) Cultivation of quinoa (Chenopodium quinoa) under temperate climatic conditions in Denmark. Journal of Agricultural Science 122, 47–52.CrossRefGoogle Scholar
Jarvis, DE, Ho, YS, Lightfoot, DJ, Schmöckel, SM, Li, B, Borm, TJA, Ohyanagi, H, Mineta, K, Michell, CT, Saber, N, Kharbatia, NM, Rupper, RR, Sharp, AR, Dally, N, Boughton, BA, Woo, YH, Gao, G, Schijlen, EGWM, Guo, X, Momin, AA, Negrão, S, Al-Babili, S, Gehring, C, Roessner, U, Jung, C, Murphy, K, Arold, ST, Gojobori, T, van der Linden, C, van Loo, EN, Jellen, EN, Maughan, PJ and Tester, M (2017) The genome of Chenopodium quinoa. Nature 542, 307–312.CrossRefGoogle ScholarPubMed
Johansen, DA (1940) Plant Microtechnique. New York: McGraw-Hill. ed.Google Scholar
Karabourniotis, G, Liakopoulos, G, Bresta, P and Nikolopoulos, D (2021) The optical properties of leaf structural elements and their contribution to photosynthetic performance and photoprotection. Plants 10, 1455.CrossRefGoogle ScholarPubMed
Lambers, H, Chapin, FS and Pons, TL (1998) Plant Physiological Ecology. New York, NY: Springer New York.CrossRefGoogle Scholar
Manaa, A, Goussi, R, Derbali, W, Cantamessa, S, Abdelly, C and Barbato, R (2019) Salinity tolerance of quinoa (Chenopodium quinoa Willd) as assessed by chloroplast ultrastructure and photosynthetic performance. Environmental and Experimental Botany 162, 103–114.CrossRefGoogle Scholar
Marchiori, PER, Machado, EC and Ribeiro, RV (2014) Photosynthetic limitations imposed by self-shading in field-grown sugarcane varieties. Field Crops Research 155, 30–37.CrossRefGoogle Scholar
Miltphore, FL, Moorby, J and González Idiarte, H (1982) Introducción a la Fisiología de los Cultivos. Bs.As. Argentina. Hemisferio Sur.Google Scholar
Mirecki, RM and Teramura, AH (1984) Effects of ultraviolet-B irradiance on soybean. Plant Physiology 74, 475–480.CrossRefGoogle ScholarPubMed
Molas, J (2002) Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni(II) complexes. Environmental and Experimental Botany 47, 115–126.CrossRefGoogle Scholar
Munns, R (2002) Comparative physiology of salt and water stress. Plant Cell and Environment 25, 239–250.CrossRefGoogle ScholarPubMed
Murphy, J and Riley, JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.CrossRefGoogle Scholar
Nkonge, C and Ballance, GM (1982) A sensitive colorimetric procedure for nitrogen determination in micro-Kjeldahl digests. Journal of Agricultural and Food Chemistry 30, 416–420.CrossRefGoogle Scholar
Parwada, C, Mandumbu, R, Tibugari, H, Badze, D and Mhungu, S (2020) Effect of soil fertility amendment, planting density and growing season on Chenopodium quinoa Willd (Quinoa) in Zimbabwe. Cogent Food & Agriculture 6, 1–16. https://doi.org/10.1080/23311932.2020.1792668.CrossRefGoogle Scholar
Prado, FE, Hilal, MB, Albornoz, PL, Gallardo, MG and Ruiz, VE (2017) Anatomical and physiological responses of four quinoa cultivars to salinity at seedling stage. Indian Journal of Science and Technology 10, 1–12.CrossRefGoogle Scholar
Rawson, HM, Begg, JE and Woodward, RG (1977) The effect of atmospheric humidity on photosynthesis, transpiration and water use efficiency of leaves of several plant species. Planta 134, 5–10.CrossRefGoogle ScholarPubMed
Rayner, M, Sjöök, M, Timgren, A and Dejmek, P (2012) Quinoa starch granules as stabilizing particles for production of Pickering emulsions. Faraday Discussions 158, 139–155.CrossRefGoogle ScholarPubMed
Ren, B, Liu, W, Zhang, J, Dong, S, Liu, P and Zhao, B (2017) Effects of plant density on the photosynthetic and chloroplast characteristics of maize under high-yielding conditions. The Science of Nature 104, 1–11. https://doi.org/10.1007/s00114-017-1445-9.CrossRefGoogle ScholarPubMed
Ruiz, RA and Bertero, HD (2008) Light interception and radiation use efficiency in temperate quinoa (Chenopodium quinoa Willd.) cultivars. European Journal of Agronomy 29, 144–152.CrossRefGoogle Scholar
Ruiz, KB, Biondi, S, Oses, R, Acuña-Rodríguez, IS, Antognoni, F, Martinez-Mosqueira, EA, Coulibaly, A, Canahua-Murillo, A, Pinto, M, Zurita, A, Bazile, D, Jacobsen, SE and Molina Montenegro, M (2014) Quinoa biodiversity and sustainability for food security under climate change. A review. Agronomy for Sustainable Development 34, 349–359.CrossRefGoogle Scholar
Schulte, M, Offer, C and Hansen, U (2003) Induction of CO2-gas exchange and electron transport: comparison of dynamic and steady-state responses in Fagus sylvatica leaves. Trees 17, 153–163.CrossRefGoogle Scholar
Shabbir, A, Abbas, G, Asad, SA, Razzaq, H, Anwar-ul-Haq, M and Amjad, M (2021) Effects of arsenite on physiological, biochemical and grain yield attributes of quinoa (Chenopodium quinoa Willd.): implications for phytoremediation and health risk assessment. International Journal of Phytoremediation 23, 890–898.CrossRefGoogle ScholarPubMed
Shokry, AM (2016) The usage of quinoa flour as a potential ingredient in production of meat burger with functional properties. Middle East Journal of Applied Sciences 6, 1128–1137. https://www.curresweb.com/mejas/mejas/2016/1128-1137.pdf.Google Scholar
Spehar, CR and da Silva Rocha, JE (2009) Effect of sowing density on plant growth and development of quinoa, genotype 4.5, in the Brazilian savannah highlands. Bioscience Journal: BJ 25, 53–58. https://seer.ufu.br/index.php/biosciencejournal/article/view/6952/4608.Google Scholar
Stanschewski, CS, Rey, E, Fiene, G, Craine, EB, Wellman, G, Melino, VJ, Patiranage, DSR, Johansen, K, Schmöckel, SM, Bertero, HD, Oakey, H, Afzal, I, Raubach, S, Miller, N, Streich, J, Buchvaldt Amby, D, Emrani, N, Warmington, M, Moussa, MAA, Wu, D, Jacobson, D, Andreasen, C, Jung, C, Murphy, K, Bazile, D and Tester, M (2021) Quinoa phenotyping methodologies: an international consensus. Plants 10, 1759, 1–52. https://doi.org/10.3390/plants10091759.Google Scholar
Tapia, M (2015) The long journey of quinoa: who wrote its history. In Bazile, D, Bertero, HD and Nieto, C (eds). State of the Art Report on Quinoa around the World in 2013. Rome: FAO, pp. 3–9.Google Scholar
Thain, JF (1983) Curvature correction factors in the measurement of cell surface areas in plant tissues. Journal of Experimental Botany 34, 87–94.CrossRefGoogle Scholar
Thomas, EC and Lavkulich, LM (2015) Community considerations for quinoa production in the urban environment. Canadian Journal of Plant Science 95, 397–404.CrossRefGoogle Scholar
Valladares, F, Allen, MT and Pearcy, RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111, 505–514.CrossRefGoogle ScholarPubMed
Van Kleunen, M, Stephan, MA and Schmid, B (2006) [CO2]- and density-dependent competition between grassland species. Global Change Biology 12, 2175–2186.CrossRefGoogle Scholar
Villalobos, FJ, Sadras, VO and Fereres, E (2016) Plant density and competition. In Villalobos, F and Fereres, E (eds). Principles of Agronomy for Sustainable Agriculture. Cham: Springer, pp. 159–168. https://doi.org/10.1007/978-3-319-46116-8_12.CrossRefGoogle Scholar
Vogelmann, T (1989) Penetration of light into plants. Photochemistry and Photobiology 50, 895–902.CrossRefGoogle Scholar
Vogelmann, TC and Martin, G (1993) The functional significance of palisade tissue: penetration of directional versus diffuse light. Plant Cell and Environment 16, 65–72.CrossRefGoogle Scholar
Wellburn, AR (1994) The Spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.CrossRefGoogle Scholar
Xiong, D, Huang, J, Peng, S and Li, Y (2017) A few enlarged chloroplasts are less efficient in photosynthesis than a large population of small chloroplasts in Arabidopsis Thaliana. Scientific Reports 7, 5782.CrossRefGoogle ScholarPubMed