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Climatic Variation on Gas Exchange and Chlorophyll a Fluorescence in Tabebuia roseoalba and Handroanthus heptaphyllus (Bignoniaceae)

Abstract

Climatic variation throughout the day influences the ecophysiological performance of plants at different growth stages and phases. Therefore, this work aimed to evaluate the effect of climatic variation on ecophysiological aspects of T. roseoalba and H. heptaphyllus at different hours of the day and indicate the ideal time for measuring ecophysiological variables in these species. The research was carried out in a greenhouse at the forest nursery of the Federal University of Paraíba, Campus II, in the municipality of Areia, Paraíba state, Northeastern Brazil. The experimental design was completely randomized, consisting of 10 evaluation times throughout the day (from 8 am to 5 pm), with 1 h hour interval between each evaluation. Temperature and air relative humidity inside and outside the greenhouse were evaluated to understand the effect on gas exchange (net assimilation rate of CO2, stomatal conductance, transpiration rate, internal concentration of CO2, and vapor-pressure deficit) and chlorophyll a fluorescence (initial, maximum, and variable fluorescence, photochemical quenching, and electron transport rate). Data were submitted to canonical correlation analysis and principal component analysis to verify the relationship between climatic and ecophysiological variables. For both species, higher correlation was found between internal and external relative humidity with all the ecophysiological variables analyzed, except for initial fluorescence. Thus, climatic factors influenced the photosynthetic performance of T. roseoalba and H. heptaphyllus plants, and 8 am to 9 am is indicated for carrying out ecophysiological evaluations in both species.

Keywords:
abiotic factors; daily course; ipê-branco; ipê-rosa; photosynthesis; physiological responses.

HIGHLIGHTS

  • Climatic conditions influence the physiological mechanisms of species.

  • High irradiance and air temperature reduce photosynthetic performance of species.

  • The highest physiological performance of the species is between 8 am and 9 am.

HIGHLIGHTS

  • Climatic conditions influence the physiological mechanisms of species.

  • High irradiance and air temperature reduce photosynthetic performance of species.

  • The highest physiological performance of the species is between 8 am and 9 am.

INTRODUCTION

Tabebuia roseoalba (Ridl.) Sandwith is a tropical tree species that grows 7 to 3 m in height and has a stem of 40 to 50 cm in diameter [11. Camarinha C, Souza DR, Delgado DR, Reis LA, Pantoja SCS. 2015. Levantamento de espécies da família Bignoniaceae ocorrentes na Universidade Castelo Branco, Campus Realengo - RJ. Rev Eletrônica de Biologia. 2015 Jul;8(3):299-307.]. Popularly known as "ipê-branco", "pau-d'arco", and "ipê-do-cerrado", the species is widely distributed in South America, occurring in several regions of Brazil, predominantly in the semi-deciduous seasonal forests of Atlantic Forest and Cerrado, and seasonal deciduous forests of Caatinga [22. Menino GCO, Nunes YRF, Santos RM, Fernandes GW, Fernandes LA. Environmental heterogeneity and natural regeneration in riparian vegetation of the brazilian semi-arid region. Edinb J Bot. 2012 Feb;69:29-51.,33. Lohmann LG. 2020. Tabebuia in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. [Cited 2021 April 23]. Available from: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB114338.
http://floradobrasil.jbrj.gov.br/reflora...
]. Also, this species is of high economic and ecological importance, being used for landscaping due to its size and flowering over different seasons of the year, and reforestation of degraded areas due to the rapid adaptation to dry and stony soils [44. Lorenzi H. 2009. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Nova Odessa: Plantarum; 2009.].

Handroanthus heptaphyllus (Vell.) Mattos, popularly known as “ipê-rosa”, “ipê-roxo”, and “pau-d’arco”, is a native arboreal species that grows 10 to 20 m [55. Amaral JB, Martins L, Forti VA, Cícero SM, Marcos Filho J. Teste de raios X para avaliação do potencial fisiológico de sementes de ipê-roxo. Rev bras sementes. 2011 Oct;33:601-07.]. Widely distributed in Brazil, mainly in the seasonal semi-deciduous forests [66. Silva GR, Berger M, Bernardy D, Tabaldi LA, Tarouco CP, Sasso VM. Efeito do alumínio sobre variáveis morfofisiológicas e bioquímicas de Handroanthus heptaphyllus (Vell.) Mattos em sistema hidropônico. Braz J of Develop. 2020 Sep;6(9):65755-73.], this species is of high economic and ecological importance, being used in the timber industry for civil construction, due to desirable properties of its wood, such as high density and durability [77. Borges VP, Costa MAPC, Ribas RF. Emergência e crescimento inicial de Tabebuia heptaphylla (Vell.) Toledo em ambientes contrastantes de luz. Rev Árvore. 2014 Jul;38:523-31.]. It is also used in urban afforestation and restoration of forest remnants in disturbed areas, and as antitumor, antioxidant, and antidepressant agents due to is biological activity [88. Freitas AE, Machado DG, Budni J, Neis VB, Balen GO, Lopes MW, et al. Antidepressant-like action of the bark ethanolic extract from Tabebuia avellanedae in the olfactory bulbectomized mice. J Ethnopharmacol. 2013 Feb;145(3):737-45.,99. Zhang L, Tatsuno T, Hasegawa I, Tadano T, Ohta T. Furanonaphthoquinones from Tabebuia avellanedae induce cell cycle arrest and apoptosis in the human non-small cell lung cancer cell line A549. Phytochem Lett. 2015 Mar;11:9-17.].

Given the ecological importance of T. roseoalba and H. heptaphyllus, studies on their ecophysiological responses to adverse climatic factors (abiotic factors) are crucial. Climatic variation throughout the day influences the ecophysiological performance of plants in the different growth stages and phases, mainly air temperature, relative humidity, and irradiance (luminosity), the main abiotic factors that affect plant metabolism [1010. Driesen E, Van den Ende W, Proft M, Saeys W. Influence of Environmental Factors Light, CO2, Temperature, and relative humidity on stomatal opening and development: A review. Agronomy. 2020 Dec;10(12):1-28.]. Arboreal forest species, obtained from natural regeneration or seedlings, are more sensitive to climatic variations due to their intrinsic characteristics [1111. Dias D, Pagotto M, Pereira T, Ribeiro A. Estrutura arbórea e sazonalidade da cobertura do dossel em vegetação florestada e aberta no parque nacional serra de Itabaiana, Sergipe, Brasil. Ci Fl. 2017 Apr;27:719-29.]. Climatic variation can affect the physiological processes of the plants, changing photosynthesis rate and chlorophyll a fluorescence [1212. Helm LT, Shi H, Lerdau MT, Yang X. Solar-induced chlorophyll fluorescence and short-term photosynthetic response to drought. Ecol Appl. 2020 Feb;30(2):1-34.].

High irradiance is one of the main factors that interfere in the physiological and morphological processes of plants, decreasing their primary metabolism, altering photosynthetic processes, reducing energy transfer and absorption in the reaction centers, CO2 fixation, net assimilation rate of CO2, transpiration rate, and stomatal conductance [1313. Morales A, Kaiser E. Photosynthetic acclimation to fluctuating irradiance in plants. Frontiers in Plant Sci. 2020 Mar;11:1-12.]. Irradiance is not associated exclusively with the availability of energy for photosynthesis. It can also induce signals responsible for regulating physiological mechanisms through light receptors sensitive to light intensity, spectrum quality, and polarization [1414. Albuquerque TCS, Evangelista TC, Albuquerque Neto AAR. Níveis de sombreamento no crescimento de mudas de castanheira do Brasil. Agro@mbiente Online. 2015 Oct;9(4):440-45.]. Also, high temperatures can negatively affect the ecophysiological processes of plants, with photosynthesis being the most sensitive process to heat stress [1515. Szymańska R, Ślesak I, Orzechowska A, Kruk J. Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot. 2017;139:165-77.]. If severe throughout the day, heat stress can inhibit photosynthesis in minutes, reducing photosynthetic activities, affecting the intracellular concentration of CO2, stomatal opening, and transpiration rate, in addition to inhibiting electron transport and suppressing Rubisco's activation state [1616. Yamori W, Masumoto C, Fukayama H, Makino A. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J. 2012 Jul;71:871-80.].

In this context, ecophysiological studies of forest species, such as T. roseoalba and H. heptaphyllus, are essential to understand the physiological behavior, adaptation, and stabilization of these species in adverse climatic conditions. There is no information on how climatic variation affects the ecophysiological aspects of such species. This information can help to understand the dynamics of T. roseoalba and H. heptaphyllus in vegetation fragments and may contribute to the propagation and conservation of these species in disturbed areas. In this study, we hypothesize that: (1) T. roseoalba and H. heptaphyllus respond differently throughout the day; and (2) heat stress (high temperature) associated with high irradiance (photosynthetically active radiation) throughout the day reduces the plant photosynthetic performance, negatively affecting gas exchange and chlorophyll a fluorescence parameters.

Thus, this study aimed to evaluate the effect of climatic variation on ecophysiological aspects of T. roseoalba and H. heptaphyllus at different hours of the day and indicate the ideal time for measuring these ecophysiological variables.

MATERIAL AND METHODS

The research was carried out in a greenhouse at the forest nursery of the Federal University of Paraíba, Campus II, in the municipality of Areia, Paraíba state, Northeastern Brazil (6°57'59'' S, 35°42'57'' W). The region is located in the Brejo microregion and Agreste Paraibano mesoregion, where altitudes reach 400 to 600 m, temperature of 22 °C, and average annual rainfall of 1,400 mm [1717. Ribeiro JES, Barbosa AJS, Lopes SF, Pereira WE, Albuquerque MB. Seasonal variation in gas exchange by plants of Erythroxylum simonis Plowman. Acta bot bras. 2018 Apr;32:287-96.]. The climate is tropical with dry summer and autumn-winter rains, classified as As [1818. Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen's climate classification map for Brazil. Meteorol Z. 2013 Dec;22:711-28.]. During the experiment, air temperature and relative humidity were monitored daily using a digital Thermo hygrometer (MT-241A, Minipa), whose average values were 24.2 °C and 53.5%, respectively.

T. roseoalba and H. heptaphyllus seeds were obtained from the seed bank from the Center for Agricultural Sciences, Federal University of Paraíba, Areia, Paraíba, Northeastern Brazil. The selected seeds were dehiscence at the initial stage, that is, at the maturation phase. After screening manually, the seeds were exposed to shade for 24 h. Before sowing, the seeds were disinfected by immersion in a 2% sodium hypochlorite solution for 5 min.

Then the seeds were sown in 8 dm3 plastic pots filled with a substrate composed of vegetal soil and Bioplant® at a 3:1 ratio. The substrate had the following chemical attributes: 5.42 pH (H2O); 118.7 and 217.2 mg dm-3 of P and K+, respectively; 0.43, 4.62, 0.00, 3.50, 3.10, 7.58, and 12.2 cmolc dm-3 of Na+, H++Al+3, Al3+, Ca2+, Mg2+, sum of bases, and cation exchange capacity, respectively; 62.1% base saturation; and 29.86% organic matter. Five seeds were sown per pot and 30 days after emergence, a thinning was carried out leaving the most uniform seedlings. Irrigation was performed daily using the gravimetric method, by weighing the pots and maintaining the substrate at 80% field capacity [1919. Souza CC, Oliveira FA, Silva IF, Amorim Neto MS. Avaliação de métodos de determinação de água disponível e manejo da irrigação em terra roxa sob cultivo de algodoeiro herbáceo. Rev Bras Eng Agr Amb. 2000 Sep;4(3):338-42.].

The experimental design was completely randomized, consisting of ten evaluation times throughout the day (from 8 am to 5 pm), with 1 h intervals between each evaluation. For each species, 12 replicates were used, two plants per plot, totaling 24 individuals of each species.

Internal (InT) and external (ExT) temperature (°C), and internal (InRH) and external (ExRH) relative humidity of the greenhouse were monitored using a portable digital thermo-hygrometer (MT-241A, Minipa). Photosynthetically active radiation (PAR) (µmol m-2 s-1) was measured using the natural light sensor of the portable infrared gas analyzer (IRGA, LI-6400XT, LI-COR). Also, net assimilation rate of CO2 (A, µmol m-2 s-1), stomatal conductance (gs, mol m-2 s-1), transpiration rate (E, mmol of H2O m-2 s-1), internal concentration of CO2 (Ci, µmol of CO2 m-2 s-1), and vapor-pressure deficit (VPD) were analyzed using IRGA following the protocol: relative air humidity between 50 and 60%, air flow of 300 μmol s-1, CO2 concentration of 400 μmol mol-1, and natural light sensor coupled to a 6 cm2 leaf chamber.

Subsequently, chlorophyll a fluorescence parameters were measured using a fluorimeter (LI-6400-40 LCF, LI-COR) coupled to IRGA. Leaves were subjected to a saturating flash of actinic irradiation (approximately 2,500 µmol photons m-2 s-1) and a pulse of far-red light to determine initial fluorescence (F0'), maximum fluorescence (Fm'), variable fluorescence (Fv'), photochemical quenching (qP), and electron transport rate (ETR).

Ecophysiological evaluations were carried out 365 days after sowing, on days under favorable climatic conditions, with full brightness, to assess the real effect of climatic factors on plants. The measurements were performed on three healthy and fully expanded leaves located in the middle third of the plants.

Canonical Correlation Analysis (CCA) and Principal Component Analysis (PCA) were performed to evaluate correlations between the climatic (PAR, InT, ExT, InRH, and ExRH) and ecophysiological variables (A, gs, E, Ci, VPD, F0', Fm', Fv', qP, and ETR). Wilks' lambda test was performed to analyze the significance of canonical roots. Also, Pearson's correlation analysis was performed, then values were classified according to the degree of dependence of Stell and Torrie (1980). All statistical analyzes were performed in R v.4.0.3 [2020. R Core Team. 2021. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. [Cited 2021 April 23]. Available from: https://www.R-project.org/.
https://www.R-project.org...
].

RESULTS

Wilks' Lambda test revealed significant correlations between the climatic and ecophysiological variables (p <0.05). The first three canonical pairs in T. roseoalba (R2 from 0.69 to 0.97) and the first four canonical pairs in H. heptaphyllus (R2 from 0.60 to 0.96) significantly correlated (Table 1).

Table 1
Wilks’s Lambda test. R2: Canonical correlation; F: Approximate F value; DFN: numerator degrees of freedom; DFD: denominator degrees of freedom.

According to the first canonical pair, the most important climatic variables for both species were air relative humidity inside (cc = 0.68 and 0.54) and outside (cc = 0.41 and 0.45) the greenhouse, which positively correlated with internal concentration of CO2 (cc = 0.89 and 0.82), stomatal conductance (cc = 0.88 and 0.80), photochemical quenching (cc = 0.80 and 0.81), net assimilation rate of CO2 (cc = 0.79 and 0.68), vapor-pressure deficit (cc = 0.79 and 0.78 ), variable fluorescence (cc = 0.78 and 0.79), electron transport rate (cc = 0.73 and 0.55), maximum fluorescence (cc = 0.69 and 0.66), and transpiration rate (cc = 0.68 and 0.73) (Table 2). Otherwise, internal temperature (cc = -0.58 and -0.50) did not correlate with the ecophysiological variables, except by initial fluorescence (Table 2).

Table 2
Canonical correlations and canonical pairs between climatic and ecophysiological variables for Tabebuia roseoalba and Handroanthus heptaphyllus.

According to Principal Component Analysis (PCA) for T. roseoalba, the principal components 1 and 2 (PC1 and PC2) explained respectively 62.25 and 33.25% of the total inertia, which corresponded to 95.50% of data variability (Figure 1A). Air relative humidity (internal and external) positively correlated with stomatal conductance, maximum fluorescence, vapor-pressure deficit, transpiration rate, net assimilation rate of CO2, variable fluorescence, photochemical quenching, electron transport rate, and internal concentration of CO2 (Figure 1A).

For H. heptaphyllus, the main components (62.89% in PC1 and 32.15% in PC2) explained 95.04% of data variability, with positive correlations between air relative humidity (internal) and vapor-pressure deficit, stomatal conductance, maximum fluorescence, transpiration rate, net assimilation rate of CO2, variable fluorescence, photochemical quenching, and internal concentration of CO2 (Figure 1B).

In both species, the internal temperature eigenvector was positioned left side, presenting negative values, indicating this parameter distinguished from the ecophysiological variables analyzed, except for initial fluorescence (Figure 1A and B).

The ecophysiological variables in both species strong correlated (r ≥ 0.72), according to Pearson's correlation analysis, except by initial fluorescence (Figure 2A and B). In T. roseoalba, photosynthetically active radiation and air temperature (external) moderately correlated with internal concentration of CO2 (0.60 and 0.62) and electron transport rate (0.61 and 0.65) (Figure 2A). Similarly, air relative humidity (internal) moderately correlated with stomatal conductance (0.57), transpiration rate (0.56), net assimilation rate of CO2 (0.52), vapor-pressure deficit (0.52), and maximum fluorescence (0.51) (Figure 2A). In H. heptaphyllus, electron transport rate positively correlated with air temperature (external) (0.74) and photosynthetically active radiation (0.66), while internal concentration of CO2 positively correlated with photosynthetically active radiation (0.54) (Figure 2B).

The climatic variables varied throughout the day, in which photosynthetically active radiation (PAR) ranged from 49.00 µmol s-1 m-2 (5 pm) to 1486.14 µmol s-1 m-2 (12 pm) (Figure 3). Maximum temperatures of 40.8 °C (InT) and 38.6 °C (ExT) (Figure 3) were recorded in the same period as for photosynthetically active radiation, at 1 pm and 12 pm. In contrast, internal and external relative humidity drastically reduced during the highest irradiance (PAR) and air temperature (InT and ExT) periods, with minimum at 2 pm (InRH = 30%; ExRH = 32%) and maximum at 8 am and 5 pm (Figure 3).

Net assimilation rate of CO2 (A) of the species decreased significantly throughout the day, due to the increase in photosynthetically active radiation (PAR) and air temperature (InT and ExT) (Figure 4A). In T. roseoalba and H. heptaphyllus, the highest net assimilation rate of CO2 was recorded earlier in the day, at 8 am and 9 am (10.42 and 8.48 µmol m-2 s-1 in T. roseoalba, and 6.54 and 5.78 µmol m-2 s-1 in H. heptaphyllus), decreasing thereafter (Figure 4A). In both species, the lowest values were observed at 5 pm (Figure 4A). Stomatal conductance (gs) varied similarly as net assimilation rate of CO2, with maximum at 8 am in both species (0.1871 mol m-2 s-1 in T. roseoalba and 0.1128 mol m-2 s-1 in H. heptaphyllus), decreasing significantly during the day, with the lowest values recorded at 5 pm (Figure 4B).

Transpiration rate also varied similarly as net assimilation rate of CO2 and stomatal conductance in both species, with maximum earlier in the day at 8 am and 9 am, registering 3.81 and 3.11 mmol of H2O m-2 s-1 in T. roseoalba and 2.80 and 2.49 mmol of H2O m-2 s-1 in H. heptaphyllus, respectively (Figure 4C).

Internal concentration of CO2 despite behaving similarly as the other gas exchange variables, registered maximum at 9 am in both species, 317.23 µmol CO2 mol-1 in T. roseoalba and 291.05 µmol CO2 mol-1 in H. heptaphyllus (Figure 4D).

Vapor-pressure deficit (VPD) decreased with increasing irradiance and air temperature, ranging from 3.16 kPa (8 am) to 1.49 kPa (5 pm) in T. roseoalba, and from 2.77 kPa (8 am) to 1.29 kPa (5 pm) in H. heptaphyllus (Figure 4E).

Initial fluorescence (F0') increased significantly along the day in both species, with maximum at 3 pm to 5 pm, which corresponded to a decrease of 25.9% in T. roseoalba and 25.3% in H. heptaphyllus between the highest and lowest values recorded during the day (Figure 5A). Maximum was recorded at 5 pm, 564.27 electrons quantum-1 in T. roseoalba and 491.73 electrons quantum-1 in H. heptaphyllus (Figure 5A).

In contrast, maximum fluorescence (Fm') decreased throughout the day, with maximum at 8 am and 9 am and minimum at 4 pm and 5 pm in both species (Figure 5B). Values ranged from 608.44 to 1268.31 electrons quantum-1 in T. roseoalba and from 498.59 to 876.23 electrons quantum-1 in H. heptaphyllus (Figure 5B).

Variable fluorescence (Fv') behave similarly as maximum fluorescence, increasing considerably at the beginning of the day in both species, with maximum at 8 am (<InT and ExT; <PAR), 850.08 electrons quantum-1 in T. roseoalba and 508.85 electrons quantum-1 in H. heptaphyllus (Figure 5C).

Photochemical quenching (qP) decreased drastically throughout the day in both species, similarly as maximum and initial fluorescence. The highest values were recorded at 8 am (0.7067 electrons quantum-1 in T. roseoalba and 0.5793 electrons quantum-1 in H. heptaphyllus), and lowest values at 5 pm (Figure 5D). From the highest and lowest values observed, qP dropped 78.5% in T. roseoalba and 81.4% in H. heptaphyllus (Figure 5D).

Electron transport rate (ETR) decreased significantly with increasing photosynthetically active radiation and temperature, registering the lowest values at 5 pm in both species (Figure 5E). On the other hand, maximum values were recorded earlier in the day (8 am) (89.28 electrons quantum-1 in T. roseoalba and 60.70 electrons quantum-1 in H. heptaphyllus). Thus, ETR increased approximately 73% in T. roseoalba and H. heptaphyllus compared to the lowest values observed (Figure 5E).

DISCUSSION

Wilk’s Lambda and Canonical Correlation Analysis (CCA) evidenced the relationship between the groups of variables, indicating that the climatic variables (group I) correlated with the ecophysiological variables (group II) in T. roseoalba and H. heptaphyllus along the day. The importance of these groups of variables is revealed by the higher coefficients of the first canonical pair, that is, the higher the canonical coefficient the greater the importance of the variable for the group [2121. Hair Junior JF, Black WC, Babin BJ, Anderson RE, Tatham RL. Análise multivariada de dados. Porto Alegre: Bookman; 2009., 2222. Stürmer M, Busanello M, Velho JP, Heck VI, Haygert-Velho IMP. Relationship between climatic variables and the variation in bulk tank milk composition using canonical correlation analysis. Int J Biometeorol. 2018 Sep;62(9):1663-74.].

Regarding the internal and external environmental variables during the day, previous works found similar results to the present study, observing maximum photosynthetically active radiation from 11 am to 1 pm, and maximum air temperature from 1 pm to 3 pm [2323. Caron BO, Perrando ER, Schmidt D, Manfron PA, Behling A, Elli EF, et al. Relações fisiológicas em mudas de pata-de-vaca (Bauhinia forficata Link). Rev bras plantas med. 2014 Apr;16(2):196-201.,2424. Caron BO, Schneider JR, Elli EF, Eloy E, Souza VQ. Physiological relationships in Aleurites fordii Hemsl. seedlings. Rev Árvore. 2017 May;41:2-7.,2525. Ribeiro JES, Figueiredo FRA, Coêlho ES, Albuquerque MB, Pereira WE. Environmental factors variation in physiological aspects of Erythroxylum pauferrense. Bosque. 2020 May;41(2):157-64.]. Such an increase in PAR and air temperature possibly decreased air relative humidity throughout the day, in the hottest hours (11 am to 1 pm) [2626. Dalmago GA, Heldwein AB, Nied AH, Grimm EL, Pivetta CR. Maximum evapotranspiration of sweet pepper in plastic greenhouse as a function of solar radiation, temperature, relative humidity and water vapor pressure deficit of the air. Cienc Rural. 2006 May;36:785-92.]. Photosynthetically active radiation together with other climatic factors, such as high temperature, can regulate and alter the mechanisms for the photosynthetic process of plants [2727. Balfagón D, Zandalinas SI, Mittler R, Gómez-Cadenas A. High temperatures modify plant responses to abiotic stress conditions. Physiol Plant. 2020 Jun;170:335-44.].

During the day, due to increasing air temperature (external and internal) and photosynthetically active radiation (PAR), both species reduced the assimilation rate of CO2 (A), stomatal conductance (gs), transpiration (E), internal concentration of CO2 (Ci), and vapor-pressure deficit (VPD). Decreased gas exchange throughout the day indicates the negative effect of high temperature and irradiance on plants, decreasing ATP and NADPH concentration due to a reduction in the photosynthesis photochemical stage [2828. Goraya GK, Kaur B, Asthir B, Bala S, Kaur G, Farooq M. Rapid injuries of high temperature in plants. J Plant Biol. 2017 Aug;60:298-305.,2929. Gómez R, Vicino P, Carrillo N, Lodeyro AF. Manipulation of oxidative stress responses as a strategy to generate stress-tolerant crops. From damage to signaling to tolerance. Crit Rev Biotechnol. 2019 Apr;39:693-708.].

Results showed that A, gs, and E in both species were strongly correlated, and acting as mechanisms and strategies responsible for regulating temperature and water content in the leaves, depending directly on stomatal opening and closure [3030. Chaves MM, Costa JM, Zarrouk O, Pinheiro C, Lopes CM, Pereira JS. Controlling stomatal aperture in semi-arid regions - The dilemma of saving water or being cool? Plant Sci. 2016 Oct;251:54-64.]. Decreased E under high temperature and irradiance possibly occurred due to the lower efficiency of leaves to assimilate and store CO2, since the competition between CO2 and H2O molecules probably reduced water loss by the stomata during this period [3131. Lambers H, Oliveira RS. 2019. Plant Physiological Ecology. New York: Springer; 2019.].

A high internal concentration of CO2 (Ci) earlier in the day possibly occurred due to higher assimilation of CO2 during this period, indicating that CO2 was being fixed by the enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) [3232. Busch FA. Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism. Plant J. 2020 Jan;101:919-39.]. Therefore, stomatal closure during the hottest hours of the day reduced Ci, thus causing a diffusive resistance of CO2 in the leaves throughout the day [3333. Nadal M, Flexas J. Mesophyll conductance to CO2 diffusion: Effects of drought and opportunities for improvement. In: Water Scarcity and Sustainable Agriculture in Semiarid Environment (IFG Tejero, VHD Zuazo, eds.). Academic Press, 2018. 403-38.]. Also, the decrease in vapor-pressure deficit (VPD) throughout the day may be associated with a lower stomatal opening during the warmer period, to reduce the gas exchange flow in the leaves [3434. Souza ER, Amaro ACE, Santos LS, Ono EO, Rodrigues JD. Fenologia e trocas gasosas da videira cv. Sweet Sunshine em clima semiárido. Comun Sci. 2016 Jul;7:319-33.].

Chlorophyll a fluorescence variables showed similar behavior to gas exchange variables in both species, except for initial fluorescence (F0'), which behaved oppositely. Higher F0' throughout the day under high temperature and radiation possibly indicate limitations in the transfer of energy to the reaction centers of photosystem II [3535. Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, et al. Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res. 2017 Nov;132:13-66.]. Under unfavorable climatic conditions, as we observed during the hottest hours of the day in the present study, F0' increased thereby influencing the structure of PSII photosynthetic pigments [3636. Perboni AT, Martinazzo EG, Silva DM, Bacarin MA. Baixas temperaturas sobre a fluorescência da clorofila a em plantas de diferentes híbridos de canola. Cienc Rural. 2015 Oct;45:215-22.]. On the other hand, the reduction in maximum fluorescence (Fm') during this period may have altered the photochemical activity of the plant, since high Fm' directly influence on energy transfer, which is used to reduce NADPH, ATP, and ferredoxin and thus increase the assimilation of CO2 by the leaves [3737. Silva FG, Dutra WF, Dutra AF, Oliveira IM, Figueiras LMB, Melo AS. Trocas gasosas e fluorescência da clorofila em plantas de berinjela sob lâminas de irrigação. Rev Bras Eng Agr Amb. 2015 Sep;19:946-52.]. In contrast, higher variable fluorescence (Fv') earlier in the day possibly improved the capacity to transfer electrons captured by the photosynthetic pigment molecules [3838. Souza JTA, Ribeiro JES, Ramos JPF, Sousa H, Araújo JS, Lima GFC, et al. Rendimento quântico e eficiência de uso da água de genótipos de palma forrageira no Semiárido brasileiro. Arch de Zootec. 2019 Apr;68(262):268-73.].

Photochemical quenching (qP) decreased proportionally with increasing temperature. The number of open reaction centers was thus reduced preventing greater light capture during this period along the day [3939. Osmond CB, Chow WS, Robinson SA. 2021. Inhibition of non-photochemical quenching increases functional absorption cross-section of photosystem II as excitation from closed reaction centres is transferred to open centres, facilitating earlier light saturation of photosynthetic electron transport. Funct Plant Biol. 2021 Mar; Forthcoming.]. This trend indicates the lower photochemical quenching efficiency of the studied species, with similar behavior to net assimilation rate of CO2 (A). Stresses caused by climatic variation provide deleterious effects on the photosynthetic mechanisms of plants. In addition, it reduces the plant photochemical efficiency and other ecophysiological parameters, such as photochemical dissipation and electron transport rate (ETR) in the photosynthetic apparatus [4040. Grime JP. Stress Physiology. In: Environmental Plant Physiology: Botanical strategies for a climate smart planet. Taylor & Francis Group, 2020. 139-66.,4141. Kochhar SL, Gujral SK. Plant Physiology: Theory and Applications. New York: Cambridge University Press; 2020.]. High electron transport rate (ETR) indicates greater use of light energy for photochemical processes, in addition to improving photosynthesis [4242. Rodrigues TB. Fluorescência da clorofila e emissões de isopreno em função do aumento da temperatura em indivíduos de Vismia guianensis na Amazônia Central. Dissertação do Programa de Pós-Graduação em Ciências de Florestas Tropicais do Instituto Nacional de Pesquisas da Amazônia. Manaus - AM. 2019,49p.], as we observed in the present study for both species.

Here we observed that the climatic variables evaluated throughout the day influenced the ecophysiological performance of T. roseoalba and H. heptaphyllus. The ecophysiological variables were affected because they were evaluated in a greenhouse (protected environment). In this environment, the air evaporative demand was satisfactory, and evapotranspiration was reduced due to decreased wind speed and solar radiation provided by the greenhouse covering, providing favorable conditions for carrying out climatic and ecophysiological assessments.

CONCLUSION

T. roseoalba and H. heptaphyllus changed their physiological mechanisms due to environmental conditions throughout the day; The ecophysiological behavior of the species is highly dependent on climatic conditions; High irradiance and air temperature negatively influenced the physiological behavior of T. roseoalba and H. heptaphyllus, drastically reducing their photosynthetic performance; The appropriate time to carry out gas exchange and chlorophyll a fluorescence evaluations in T. roseoalba and H. heptaphyllus is from 8 am to 9 am.

Acknowledgments:

To Forest Nursery, from the Federal University of Paraíba, Campus II, for the supply of seeds.

  • ERRATUM

    In the Article “Climatic Variation on Gas Exchange and Chlorophyll a Fluorescence in Tabebuia roseoalba and Handroanthus heptaphyllus (Bignoniaceae)” DOI number: https://doi.org/10.1590/1678-4324-2022210338, published in the journal Brazilian Archives of Biology and Technology, vol. 65, page 1.
    That read:
    “(…) Air relative humidity (internal and external) positively correlated with stomatal conductance, maximum fluorescence, vapor-pressure deficit, transpiration rate, net assimilation rate of CO2, variable fluorescence, photochemical quenching, electron transport rate, and internal concentration of CO2 (Figure 1A).
    Read:
    “(…) Air relative humidity (internal and external) positively correlated with stomatal conductance, maximum fluorescence, vapor-pressure deficit, transpiration rate, net assimilation rate of CO2, variable fluorescence, photochemical quenching, electron transport rate, and internal concentration of CO2 (Figure 1A).
    Figure 1
    Principal Component Analysis (PCA) for climatic and ecophysiological variables in Tabebuia roseoalba (a) and Handroanthus heptaphyllus (b).”
    and
    That read:
    “(…) In H. heptaphyllus, electron transport rate positively correlated with air temperature (external) (0.74) and photosynthetically active radiation (0.66), while internal concentration of CO2 positively correlated with photosynthetically active radiation (0.54) (Figure 2B).
    Read:
    “(…) In H. heptaphyllus, electron transport rate positively correlated with air temperature (external) (0.74) and photosynthetically active radiation (0.66), while internal concentration of CO2 positively correlated with photosynthetically active radiation (0.54) (Figure 2B).
    Figure 2
    Pearson's correlation coefficients between climatic and ecophysiological variables in Tabebuia roseoalba (a) and Handroanthus heptaphyllus (b) plants.”
    and
    That read:
    “(…) Maximum temperatures of 40.8 °C (InT) and 38.6 °C (ExT) (Figure 3) were recorded in the same period as for photosynthetically active radiation, at 1 pm and 12 pm. In contrast, internal and external relative humidity drastically reduced during the highest irradiance (PAR) and air temperature (InT and ExT) periods, with minimum at 2 pm (InRH = 30%; ExRH = 32%) and maximum at 8 am and 5 pm (Figure 3).
    Read:
    “(…) Maximum temperatures of 40.8 °C (InT) and 38.6 °C (ExT) (Figure 3) were recorded in the same period as for photosynthetically active radiation, at 1 pm and 12 pm. In contrast, internal and external relative humidity drastically reduced during the highest irradiance (PAR) and air temperature (InT and ExT) periods, with minimum at 2 pm (InRH = 30%; ExRH = 32%) and maximum at 8 am and 5 pm (Figure 3).
    Figure 3
    Photosynthetically active radiation (PAR), internal (InT) and external (ExT) temperature, and internal (InRH) and external (ExRH) relative humidity of the environment (greenhouse) during the experiment.”
    and
    That read:
    “(…) Vapor-pressure deficit (VPD) decreased with increasing irradiance and air temperature, ranging from 3.16 kPa (8 am) to 1.49 kPa (5 pm) in T. roseoalba, and from 2.77 kPa (8 am) to 1.29 kPa (5 pm) in H. heptaphyllus (Figure 4E).
    Read:
    “(…) Vapor-pressure deficit (VPD) decreased with increasing irradiance and air temperature, ranging from 3.16 kPa (8 am) to 1.49 kPa (5 pm) in T. roseoalba, and from 2.77 kPa (8 am) to 1.29 kPa (5 pm) in H. heptaphyllus (Figure 4E).
    Figure 4
    Net assimilation rate of CO2 (A) (a), stomatal conductance (gs) (b), transpiration rate € (c), internal concentration of CO2 (Ci) (d), and vapor-pressure deficit (VPD) (e) in Tabebuia roseoalba (●) and Handroanthus heptaphyllus (○) plants along the day. “
    and
    That read:
    “(…) On the other hand, maximum values were recorded earlier in the day (8 am) (89.28 electrons quantum-1 in T. roseoalba and 60.70 electrons quantum-1 in H. heptaphyllus). Thus, ETR increased approximately 73% in T. roseoalba and H. heptaphyllus compared to the lowest values observed (Figure 5E).
    Read:
    “(…) On the other hand, maximum values were recorded earlier in the day (8 am) (89.28 electrons quantum-1 in T. roseoalba and 60.70 electrons quantum-1 in H. heptaphyllus). Thus, ETR increased approximately 73% in T. roseoalba and H. heptaphyllus compared to the lowest values observed (Figure 5E).
    Figure 5
    Initial fluorescence (F0') (a), maximum fluorescence (Fm') (b), variable fluorescence (Fv') (c), photochemical dissipation (qP) (d), and electron transport rate (ETR) (e) in Tabebuia roseoalba (●) and Handroanthus heptaphyllus (○) plants along the day.”

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Edited by

Editor-in-Chief: Alexandre Rasi Aoki
Associate Editor: Marcos Pileggi

Publication Dates

  • Publication in this collection
    28 Mar 2022
  • Date of issue
    2022

History

  • Received
    24 May 2021
  • Accepted
    05 Oct 2021
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