Genetic variability of the initial growth of Eugenia dysenterica DC.: implications for conservation and breeding¹

Variabilidade genética do crescimento inicial de Eugenia dysenterica DC.: implicações para conservação e melhoramento genético

ABSTRACT

Eugenia dysenterica DC. is a native tree from the Brazilian Savanna known as a genetic resource for its fruits and culinary potential. The knowledge on the genetic variability of agronomic traits is important to support studies on its conservation and domestication. This study aimed to estimate the quantitative genetic parameters of initial growth traits among and within E. dysenterica subpopulations, in provenance and progeny testing, and establish a germplasm collection representative of the species distribution. For that, 25 natural subpopulations were sampled and, within each subpopulation, six mother trees. The progenies were sown in a nursery, in a randomized complete blocks design consisting of 150 progenies, four replications and five plants per plot. The analysis of variance of the initial development traits revealed a greater variability among the progenies within the subpopulation than that observed among the subpopulations. The aboveground biomass represented only 15 % of the total biomass, a recurrent characteristic in Brazilian Savanna species. The estimated heritability and coefficients of genetic variation presented selection potential for the initial development traits, which are important for commercial seedlings production. An in vivo ex situ germplasm collection was established for conservation and breeding purposes, using a sample of four plants from each progeny.

KEYWORDS:
Cagaita; progeny test; Brazilian Savanna; genetic resources

RESUMO

Eugenia dysenterica DC. é uma árvore nativa do Cerrado conhecida como recurso genético por seus frutos e potencial culinário. O conhecimento da variabilidade genética de características agronômicas é importante para subsidiar pesquisas sobre a sua conservação e domesticação. Objetivou-se estimar os parâmetros genéticos quantitativos das características iniciais de crescimento entre e dentro de subpopulações de E. dysenterica, em teste de procedências e progênies, e estabelecer uma coleção de germoplasma representativa da distribuição da espécie. Para isso, 25 subpopulações naturais foram amostradas e, dentro de cada subpopulação, 6 árvores matrizes. As progênies foram semeadas em viveiro, em delineamento de blocos ao acaso constituído de 150 progênies, quatro repetições e cinco plantas por parcela. A análise de variância de caracteres do desenvolvimento inicial revelou maior variabilidade entre progênies dentro da subpopulação do que a observada entre as subpopulações. A biomassa acima do solo representou apenas 15 % da biomassa total, característica recorrente em espécies do Cerrado. A herdabilidade estimada e os coeficientes de variação genética apresentaram potencial de seleção para os caracteres de desenvolvimento inicial, importantes para a produção comercial de mudas. Uma coleção de germoplasma in vivo ex situ foi estabelecida para fins de conservação e melhoramento, utilizando-se uma amostra de quatro plantas de cada progênie.

PALAVRAS-CHAVE:
Cagaita; teste de progênies; Cerrado; recursos genéticos

INTRODUCTION

Eugenia dysenterica DC., Myrtaceae, is a fruit tree species with potential for commercial exploitation as processed or fresh food (Araújo et al. 2019), as well as a source of bioactive components (Justino et al. 2020). Its fruit, known as cagaita, is harvested by local collectors in the Cerrado biome (Brazilian Savanna) (Guéneau et al. 2020), a global conservation hotspot (Myers et al. 2000).

There is a growing market demand for native socio-biodiverse products such as cagaita. However, the expansion of the production chain is limited by problems such as obtaining raw material in a sustainable manner (Guéneau et al. 2020). Conservation and domestication strategies are essential to avoid the predatory extraction and encourage the commercial exploitation of the species. Due to its high genetic variability and fruit yield, E. dysenterica is a good target for breeding programs (Aguiar et al. 2009).

Although the species is allogamous (Rodrigues et al. 2016), it also exhibits self-compatibility, with the self-fertilization of some seeds confirmed by manual pollination (Proença & Gibbs 1994). Its flowering strategy is synchronous and abundant, with pollination performed mainly by bees (Proença & Gibbs 1994).

Regional studies have assessed the genetic variability of E. dysenterica for initial growth (plant height and stem diameter) (Trindade & Chaves 2005, Aguiar et al. 2009), with others investigating breeding purposes (Chaves et al. 2011, Silva et al. 2017, Novaes et al. 2018). However, there are no large-scale studies on initial growth traits with extensive sampling in the Brazilian Savanna.

Knowledge on the species’ genetic variability for different growth traits is important for domestication purposes, to select economically beneficial genotypes, and for conservation, to visualize the diversity among families and access its genetic vulnerability. Genetic variability is essential to ensure the species’ resistance to environmental changes. Genetic uniformity causes vulnerability in both cultivated and natural populations because it increases the chance of inbreeding depression and loss of alleles in each generation, and reduces the alternatives for natural or artificial selection. As such, studies on phenotypic traits in progeny tests are important for future predictions of genetic differentiation. Genetic variability is relevant, and the climate changes predicted for the coming decades highlight the importance of genetic resources conservation (Swarup et al. 2021).

Establishing native fruit germplasms of species threatened by anthropic pressure is the foundation for exploring genetic diversity and necessary for domestication and conservation (Diniz-Filho et al. 2020). The Universidade Federal de Goiás (UFG) (Goiânia, Goiás state, Brazil) has an in vivo E. dysenterica collection, sampled from 23 subpopulations in southeastern, northern and northeastern Goiás state (Trindade & Chaves 2005, Aguiar et al. 2009, Chaves & Telles 2010). Despite its importance, the collection contains no germplasm from other regions of the species’ natural distribution.

This study aimed to assess the quantitative genetic variability for initial growth stages within and among E. dysenterica subpopulations, and compile a germplasm collection to support breeding and conservation programs for the species.

MATERIAL AND METHODS

Provenance and progeny tests were conducted using seeds sampled from 25 subpopulations across the species’ distribution in the Cerrado biome (Figure 1). Six mother trees were sampled for each subpopulation, generating 150 open-pollinated progenies (maternal families). The collected fruits were transported from the field in a cooler box filled with ice chips and refrigerated for 5 to 15 days, until physical characterization of fruit and seed traits (Novaes et al. 2018). The seeds were then sown for a nursery experiment.

A completely randomized blocks design was used, with 150 treatments (maternal families). Four replicates and five seeds per plot were used for each treatment, resulting in 20 plants per progeny, totaling 3,000 planted seeds. Seeds were individually sown in 1 L plastic bags filled with a mixture of soil, sand and manure (1:1:1). The experiment was carried out from November 2011 to November 2013, in a nursery of the Universidade Federal de Goiás, in Goiânia, Goiás state, Brazil (16º36’S, 49º17’W and altitude of 736 m). The climate in the region is classified as Aw, according to the Köppen-Geiger system (Alvares et al. 2013), hot and semi-humid, with a well-defined dry season from May to September, with average annual temperature of 22.1 ºC, average minimum and maximum temperatures of 15.2 ºC and 30.4 ºC, respectively, and average annual rainfall of 1,495 mm (Casaroli et al. 2018). In the absence of rainfall, manual irrigation was performed. Weeds were removed manually when present.

The following traits were evaluated between 1 and 20 months after sowing (Table 1): emergence percentage, days to emergence, emergence speed, initial and final plant height, initial and final stem diameter, leaf length and width, and number of leaves. Diameter was determined using a digital caliper. Leaf and root height and length were obtained with a millimeter ruler and expressed in cm. The growth rates for plant height and stem diameter were estimated using the linear regression coefficient of the data obtained from eight measurements during the seedling development. At 12 months, the root fresh and dry mass, aboveground fresh and dry mass, and root and shoot length were measured for each progeny, in four plants randomly chosen from different blocks. Next, assessments were carried out with 4 plants per plot. The leaf area was calculated according to Oga & Fonseca (1994) for E. dysenterica. The relationships among the traits were determined by the Spearman’s correlation, with significance assessed using the Student’s t test, including some fruit and seed traits from a previous study (Novaes et al. 2018).

Figure 1
Location of 25 Eugenia dysenterica DC. subpopulations used in provenance and progeny testing. The lines indicate Brazilian states borders. The Cerrado biome (Brazilian Savanna) is highlighted in orange.

Table 1
Date of quantitative traits assessments in a progeny test of Eugenia dysenterica DC.

Trait	Date	Number of evaluations
Emergence percentage	15 Nov. 2011 to 15 Apr. 2012	3,000
Days to emergence	15 Nov. 2011 to 15 Apr. 2012	2,461
Initial plant height (cm)	01 Feb. 2012	2,419
Plant height (cm)	15 Feb. 2012	2,438
Plant height (cm)	29 Feb. 2012	2,451
Plant height (cm)	29 Mar. 2012	2,451
Plant height (cm)	02 May 2012	2,475
Plant height (cm)	18 June 2012	2,475
Plant height (cm)	30 Aug. 2012	2,464
Final plant height (cm)	30 Oct. 2012	2,476
Initial stem diameter (mm)	02 Feb. 2012	1,824
Stem diameter (mm)	16 Feb. 2012	2,387
Stem diameter (mm)	01 Mar. 2012	2,415
Stem diameter (mm)	30 Mar. 2012	2,452
Stem diameter (mm)	02 May 2012	2,470
Stem diameter (mm)	11 June 2013	2,475
Stem diameter (mm)	30 Aug. 2012	2,477
Final stem diameter (mm)	31 Oct. 2012	2,475
Leaf length (cm)	18 June 2012	4,862
Leaf width (cm)	18 June 2012	4,862
Number of leaves	18 June 2012	2,462
Root fresh mass (g)	22 Nov. 2012	566
Root dry mass (g)	24 Nov. 2012	562
Aboveground fresh mass (g)	22 Nov. 2012	566
Aboveground dry mass (g)	24 Nov. 2012	563
Root length (cm)	22 Nov. 2012	566
Shoot length (cm)	22 Nov. 2012	566

The genetic parameters were estimated by analysis of variance, using the hierarchical model: $$Y_{ijk}=\mu +s_i+f_{j(i)}+b_k+e_{k(ij)}$$, where Y_ijk is the value of the variable Y from progeny j, within subpopulation i in block k; μ the general mean; s_i the random effect of subpopulation i, i = 1, 2, ..., S; f_j(i) the random effect of progeny j within subpopulation i, j = 1, 2, ..., F_i; b_k the random effect of block k, k = 1, 2,..., B; and e_k(ij) the experimental error. The coefficients of genetic variation and heritability were estimated for progenies within subpopulations. All the analyses were performed with scripts developed for the R software (R Core Team 2013).

The in vivo germplasm collection was compiled 24 months after sowing, with three plants from each progeny randomly selected from different blocks in the nursery. The experimental area consists of 3 x 2 m spacing in three completely randomized blocks, with one plant per block and 150 treatments. The soil is classified as a Red Latosol (Santos et al. 2018) or Typic Hapludox (USDA 2014), and the coordinates and climate are the same as those of the nursery. The representativeness of the germplasm collection was determined based on the effective population size, calculated using the appropriate model for the provenance and progeny design (Vencovsky et al. 2007) N_e = 2D, in which:

$$D={\theta }_P[\left(\frac{1+C_S^2}{S}\right)\left(\frac{S^{\ast }}{S^{\ast }-1}\right)-\frac{1}{S^{\ast }-1}-\frac{1+C_m^2}{M}]+{\theta }_M(\frac{1+C_m^2}{M}-\frac{1}{N})+\frac{1+F}{2N}$$

where θ_P is the genetic divergence among subpopulations, equivalent to the Wright’s F_ST ; θ_M the remote coancestry coefficient of individuals within progenies and subpopulations, calculated as $${\theta }_M={\theta }_M^{\mathrm{\prime }}+{\theta }_P(1-{\theta }_M^{\mathrm{\prime }});{\theta }_M^{\mathrm{\prime }}$$ the recent coancestry coefficient among individuals within families; N, M and S the total number of plants, families and subpopulations, respectively; F the total fixation index equivalent to the Wright’s F_IT ; C_S and C_m the number of plants and coefficients of variation per subpopulation and family, respectively; S* the supposed number of subpopulations in nature, considered S* ≈ ∞ for E. dysenterica, making $$\left[S^{\ast }/(S^{\ast }-1)\right]=1$$ and $$1/(S^{\ast }-1)=0$$. The molecular genetic parameters for the Wright´s equivalents were estimated in a previous study (F = 0.3215; θ_p = 0.198; θ_m´ = 0.153), with a sample of the same seedlings (Boaventura-Novaes et al. 2018).

RESULTS AND DISCUSSION

The sources of variation differed significantly for emergence percentage, days to emergence and emergence speed (Table 2). The average germination percentage was 82 %. The literature reports several values for the emergence percentage of E. dysenterica, some of which were homogeneous among treatments (Oga et al. 1992, Mota et al. 2018) and others heterogeneous within a single subpopulation (Duarte et al. 2006), varying from 80.6 (Souza et al. 2001) to 99 % (Mota et al. 2018). As shown in these articles, emergence percentages and number of days to emergence are homogeneous among the studies, even for different populations and environmental sowing conditions.

Table 2
Analysis of variance, coefficients of experimental variation (CVe), genetic variation (CVg) and heritability on a mean basis ($$h_m^2$$) for phenotypic growth traits of 25 subpopulations of Eugenia dysenterica DC. provenance and progeny testing.

Source of variation	DF	Mean square
		EP	DE	ES	IH	FH	HR	ID	FD	DR
Blocks	3	306.91*	78.12ns	0.003**	0.25ns	18.01** *	0.19** *	0.046** *	0.528** *	0.007** *
Subpopulations	24	455.14*	375.11*	0.012** *	3.27** *	13.42** *	0.04** *	0.052** *	0.143** *	0.001** *
Progenies/subpopulations	123	256.02** *	214.61** *	0.006** *	0.71** *	2.33** *	0.01*	0.016** *	0.042** *	0.0003**
Error	427	89.21	54.43	0.001	0.14	0.76	0.01	0.004	0.014	0.0002
Mean		82.03	32.13	2.93	2.29	4.53	0.25	0.89	1.13	0.01
CVe		4.75	3.44	18.15	40.28	40.63	39.81	16.20	20.57	110.66
CVg		21.16	17.35	1.22	21.29	14.16	9.26	6.20	7.55	26.56
$$h_m^2$$		0.82	0.65	0.86	0.80	0.68	0.23	0.75	0.66	0.36

• ^*
  ,
• ^**
  ,
• ^***
  and
• ^ns
  p-value < 5 %, 1 % and 0.1 % and non-significant, respectively, by the F test. EP: emergence percentage; DE: days to emergence; ES: emergence speed; IH: initial height (cm); FH: final height (cm); HR: height growth rate; ID: initial diameter (cm); FD: final diameter (cm); DR: diameter growth rate.

The seedling emergence began at 19 days after sowing. The latest emergence was observed at 198 days after sowing in the subpopulation 3 (Catalão, GO). In 42 days, 75 % of all the seedlings had emerged. Similar estimates have been reported for this trait in assessments conducted under different environments (Souza et al. 2001, Martinotto et al. 2007, Nunes et al. 2020). Studies testing different substrates (Souza et al. 2001, Nunes et al. 2020), presence of light and seed teguments in vitro (Martinotto et al. 2007) reported results comparable to those obtained here. The recalcitrant seeds and short period of favorable environmental conditions before the end of the rainy season resulted in an evolutionary investment in rapid seedling establishment. The fruits ripened between October and November, coinciding with the rainy season. Seedlings must be established by mid-April, when the dry season begins in the Cerrado biome. A previous study demonstrated that the uniform selection may be the cause of the homogeneity observed (Boaventura-Novaes et al. 2018).

The subpopulation sampling chronology was not related to germination percentage, confirmed by non-significant correlations with seed storage time (data not shown). Thus, the fruit storage conditions were adequate to preserve the seeds for 40 days without loss of viability. A low storage temperature was previously recommended by Farias Neto et al. (1991). Andrade et al. (2003) detected a complete loss of viability in E. dysenterica seeds at moisture levels between 18 and 22 %. Seed recalcitrance is a characteristic of several fruit species from the Cerrado biome, such as Hancornia speciosa, Campomanesia adamantium, Eugenia klotzschiana, Mauritia flexuosa and Brosimum gaudichaudii (Brasil 2016). As such, the storage methodology used here can be applied to seeds that are sensitive to desiccation, such as E. dysenterica.

The emergence speed, which reflects the germination vigor, is positively correlated with seed mass and longitudinal and transverse diameters (Figure 2). Larger seeds also exhibit a greater germination vigor. Since the seedling growth is slow and irregular in the field (Souza et al. 2002), an indirect selection of seeds with a greater mass may result in a faster seedling development. The heritability for emergence percentage (0.82) and days to emergence (0.65) (Table 2) suggest the possibility of selecting for genetic gains.

The coefficients of genetic variation (CVg) for emergence time and percentage were relatively high, when compared to the values obtained in cultivated species (Table 2). Fruit ripeness may also explain the variability observed in early seedling development. The fruits were harvested at different maturation stages, characterizing a maternal effect. This characteristic influenced the dormancy and initial development of another fruit from the same genus, namely Eugenia uniflora L. (Antunes et al. 2012).

For seedling height and stem diameter, there was a significant variability among the subpopulations and progenies within subpopulations (Table 2). On average, the subpopulation 23 (Britânia, GO) had the smallest seedlings, and the subpopulations 1, 2 and 21 (Bambuí, MG; Luz, MG; and Cocalinho, MT, respectively) the largest ones. The coefficient of genetic variation was higher for diameter than for height growth rate (Table 2). The higher the CVg, the better the traits’ selection response. Thus, the initial height and stem diameter growth rates are more favorable for early selection. Trees typically take several years to complete a selection cycle, making it difficult for breeders. However, in the event of significant correlations between initial growth traits and yield, these indirect traits may be combined into an index that enables early selection (Padi et al 2012).

Maternal effects may have a considerable influence on estimating initial genetic variability, since both the seedling height and stem diameter were significantly and positively correlated with fruit and seed size and mass (Figure 2). Considering maternal effects, the accuracy of the genetic effects for fruit and seed traits may be lower, even in studies resulting from a progeny test (Roach & Wulff 1987), because the maternal genotype or phenotype may exert a causal influence on phenotypic variability in offspring. Given that the timing and amount of fruit production vary among E. dysenterica trees (Souza et al. 2013), it would be relevant to determine whether early plant growth and development are associated with fruit production, when they reach reproductive maturity.

Interestingly, the stem diameter growth rate was negative for 16.38 % of the progenies, considering the measurements taken between February and October, i.e., 3 to 11 months after planting. The last two measurements (August and October), at the peak of the dry season, contributed to the negative growth rate in these progenies. Stem diameter is sensitive to water levels, which can be modulated by turgor pressure, osmotic potential and mainly by xylem water potential (Génard et al. 2001). Diameter may vary according to the stem water content, even over a one-day period (Schepper et al. 2012). Low air humidity causes leaf water loss, creating a negative pressure that can shrink the plant stem. Although the E. dysenterica seedlings were irrigated daily, the dry weather and low humidity between May and September, typical of the Cerrado biome, may have caused the decline in stem diameter observed in some progenies.

There were significant differences among progenies and subpopulations for number of leaves and leaf area (Table 3). The results demonstrate a high heterogeneity for most of the evaluated traits. The highest CVg was recorded for fresh and dry mass and the lowest one for leaf-related traits. Heritability ranged from 0.04 for root length to 0.78 for leaf width (Table 3).

Figure 2
Fruit, seed and seedling traits correlations heatmap of Eugenia dysenterica DC. DR: diameter growth rate; HR: height growth rate; ID: initial diameter; IH: initial height; RD: root dry mass; RF: root fresh mass; AD: aboveground dry mass; AF: aboveground fresh mass; FD: final diameter; FH: final height; SL: shoot length; LF: fruit longitudinal length; TF: fruit transverse diameter; FM: fruit mass; LS: seed longitudinal diameter; TS: seed transverse diameter; SM: seed mass; LL: leaf length; LW: leaf width; LA: leaf area; RL: root length; LN: leaf number; DE: days to emergence; PE: emergence percentage; NS: number of seeds per fruit.

During the first dry season, before the plants lost their leaves, the number of leaves ranged from 1 to 10, with most seedlings displaying 2. The leaf area ranged from small (0.04 cm²) to large (19.40 cm²). The subpopulations 8 and 10 (Pirapora, MG; and Brasilândia de Minas, MG) had a higher average number of leaves and, consequently, a larger leaf area. The subpopulation 21 (Cocalinho, MT) obtained the lowest average values for aboveground mass, leaf length, number of leaves and leaf area.

The underground biomass represented 85 % of the total biomass, on average. Like other native plants from the Cerrado biome, E. dysenterica is exposed to extended periods of water deficit, requiring mechanisms to capture water at greater depths. Biomass allocation to the roots may also be an adaptive strategy for the recurring fires in this biome (Tomlinson et al. 2012). A greater biomass allocation to the roots, if compared to shoots, is an adaptive characteristic retained by uniform selection, whereby the selection pressure to maintain plants under regrowth conditions allows individuals to survive until conditions in the Cerrado biome become favorable again during the rainy season (Boaventura-Novaes et al. 2018).

Table 3
Leaf and root traits analysis of variance, coefficients of experimental variation (CVe), genetic variation (CVg) and heritability on a mean basis ($$h_m^2$$) for provenance and progeny testing of 25 Eugenia dysenterica DC. subpopulations.

Source of variation	DF	Mean squares
		LA	LL	LW	NL	RD	AD	RF	AF	RL	SL
Blocks	3	10.94** *	2.21** *	0.27ns	2.29** *	2.63** *	0.22** *	9.08** *	0.72** *	28.95ns	8.56** *
Subpopulations	24	19.66** *	3.58** *	0.72** *	1.74** *	1.07** *	0.04*	1.73*	0.10ns	185.90** *	13.25** *
Progenies/subpopulations	123	4.84** *	0.72** *	0.20ns	0.59** *	0.52** *	0.02** *	1.02** *	0.06**	95.04ns	3.49** *
Error	425	1.19	0.19	0.45	0.33	0.24	0.01	0.49	0.04	91.37	1.68
Mean		4.76	3.92	1.64	2.77	1.09	0.18	1.58	0.30	27.61	6.32
CVe		19.63	10.12	10.79	9.86	54.82	72.29	52.50	76.46	35.44	25.57
CVg		7.05	9.41	12.17	7.23	24.74	26.88	23.55	24.78	3.54	10.86
$$h_m^2$$		0.74	0.74	0.78	0.27	0.53	0.42	0.52	0.34	0.04	0.52

• ^*
  ,
• ^**
  ,
• ^***
  and
• ^ns
  p-value < 5 %, 1 % and 0.1 %, and non-significant, respectively, by the F test; LA: leaf area (cm²); LL: leaf length (cm); LW: leaf width (cm); NL: number of leaves; RD: root dry mass (g); AD: aboveground dry mass (g); RF: root fresh mass (g); AF: aboveground fresh mass (g); RL: main root length (cm); SL: shoot length (cm).

An in vivo ex situ germplasm collection was planted in the experimental area of the Universidade Federal de Goiás, with a sample of three plants from each of the 150 progenies studied here (N = 450 trees). The recalcitrant nature of E. dysenterica makes its conservation in seed banks unviable. Thus, in vivo conservation has become the standard for ex situ germplasms of the species.

The estimated effective size of the germplasm collection was N_e ≅ 56, with the entire population of E. dysenterica as reference. This apparently low value is due to the strong genetic structure observed in the population, which does not meet the conditions of panmixia (Boaventura-Novaes et al. 2018). However, this effective population size is consistent with results from other studies with species from the Brazilian Savanna, such as Hymenaea stigonocarpa (Gonçalves et al. 2019) and Dipteryx alata (Guimarães et al. 2019). This representativeness is insufficient to ensure long-term genetic conservation (Vencovsky & Crossa 2003), suggesting the importance of complementary in situ conservation. On the other hand, this germplasm collection is sufficiently representative to be used as a base population in breeding programs.

CONCLUSIONS

1. The sampled population of Eugenia dysenterica exhibits genetic variability among subpopulations and progenies within subpopulations for almost all the assessed traits. This indicates a potential for genetic gain with selection at the two hierarchical levels;

2. The indirect selection of large seeds with greater mass shortens the seedling development time in the nursery;

3. The in vivo E. dysenterica germplasm collection of the Universidade Federal de Goiás has sufficient genetic representativeness to support a pre-breeding program for the species.

ACKNOWLEDGMENTS

This study was partially financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (Capes) - Finance Code 001, and was developed in the context of the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG). L. J. C., M. P. C. T. and E. N. have been supported by a productivity grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Our current research in Genetics and Genomics is developed in the context of National Institutes for Science and Technology (INCT) in Ecology, Evolution and Biodiversity Conservation, supported by MCTIC/CNPq (Proc. 465610/2014-5) and Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG), which we gratefully acknowledge. We thank Leonardo O. S. Costa, for the figure design.

REFERENCES

• AGUIAR, A. V.; VENCOVSKY, R.; CHAVES, L. J.; MOURA, M. F.; MORAIS, L. K. Genetics and expected selection gain for growth traits in Eugenia dysenterica DC. populations. Bragantia, v. 68, n. 3, p. 629-637, 2009.
• ALVARES, C. A.; STAPE, J. L.; SENTELHAS, P. C.; MORAES, G. de; LEONARDO, J.; SPAROVEK, G. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, v. 22, n. 6, p. 711-728, 2013.
• ANDRADE, A. C. S.; CUNHA, R.; SOUZA, A. F.; REIS, R. B.; ALMEIDA, K. J. Physiological and morphological aspects of seed viability of a neotropical Savannah tree, Eugenia dysenterica DC. Seed Science & Technology, v. 31, n. 1, p. 125-137, 2003.
• ANTUNES, L. E. C.; PICOLOTTO, L.; VIGNOLO, G. K.; GONCALVES, M. A. Influence of the substrate, seed size and fruit maturation in the formation of cherry tree seedlings. Revista Brasileira de Fruticultura, v. 34, n. 4, p. 1216-1223, 2012.
• ARAÚJO, F. F.; NERI-NUMA, I. A.; FARIAS, D. de P.; CUNHA, G. R. M. C. da; PASTORE, G. M. Wild Brazilian species of Eugenia genera (Myrtaceae) as an innovation hotspot for food and pharmacological purposes. Food Research International, v. 121, n. 1, p. 57-72, 2019.
• BOAVENTURA-NOVAES, C. R. D.; NOVAES, E.; MOTA, E. E. S.; TELLES, M. P. C.; COELHO, A. S. G.; CHAVES, L. J. Genetic drift and uniform selection shape evolution of most traits in Eugenia dysenterica DC. (Myrtaceae). Tree Genetics & Genomes, v. 14, n. 5, p. 1-14, 2018.
• BRASIL. Ministério do Meio Ambiente. Espécies nativas da flora brasileira de valor econômico atual ou potencial: plantas para o futuro: Região Centro-Oeste. Brasília, DF: Ministério do Meio Ambiente, 2016.
• CASAROLI, D.; RODRIGUES, T. R.; MARTINS, A. P. B.; EVANGELISTA, A. W. P.; ALVES JÚNIOR, J. Padrões de chuva e de evapotranspiração em Goiânia, GO. Revista Brasileira de Meteorologia, v. 33, n. 2, p. 247-256, 2018.
• CHAVES, L. J.; TELLES, M. P. C. Cagaita. In: VIEIRA, R. F.; COSTA, T. S. A.; SILVA, D. B.; FERREIRA, F. R.; SANO, S. M. (ed.). Frutas nativas da Região Centro-Oeste do Brasil Brasília, DF: Embrapa Recursos Genéticos e Biotecnologia, 2010. p. 120-135.
• CHAVES, L. J.; VENCOVSKY, R.; SILVA, R. S. M.; TELLES, M. P. C.; ZUCCHI, M. I.; COELHO, A. S. G. Estimating inbreeding depression in natural plant populations using quantitative and molecular data. Conservation Genetics, v. 12, n. 2, p. 569-576, 2011.
• DINIZ-FILHO, J. A. F.; BARBOSA, A. C. D. O. F.; CHAVES, L. J.; SOUZA, K. D. S.; DOBROVOLSKI, R.; RATTIS, L.; TERRIBILE, L. C.; LIMA-RIBEIRO, M. S.; OLIVEIRA, G. de; BRUM, F. T.; LOYOLA, R. Overcoming the worst of both worlds: integrating climate change and habitat loss into spatial conservation planning of genetic diversity in the Brazilian Cerrado. Biodiversity and Conservation, v. 29, n. 5, p. 1555-1570, 2020.
• DUARTE, E. F.; NAVES, R. V.; BORGES, J. D.; GUIMARÃES, N. N. R. Germinação e vigor de sementes de cagaita (Eugenia dysenterica Mart. ex DC.) em função de seu tamanho e tipo de coleta. Pesquisa Agropecuária Tropical, v. 36, n. 3, p. 173-179, 2006.
• FARIAS NETO, A. L.; FONSECA, C. E. L.; GOMIDE, C. C. C.; SILVA, J. A. Armazenamento de sementes de cagaita (Eugenia dyzenterica DC.). Revista Brasileira de Fruticultura, v. 13, n. 2, p. 55-62, 1991.
• GÉNARD, M.; FISHMAN, S.; VERCAMBRE, G.; HUGUET, J-G.; BUSSI, C.; BESSET, J.; HABIB, R. A biophysical analysis of stem and root diameter variations in woody plants. Plant Physiology, v. 126, n. 1, p. 188-202, 2001.
• GONÇALVES, A. R.; CHAVES, L. J.; TELLES, M. P. C. Genetic variability and effective population size in Hymenaea stigonocarpa (Fabaceae) germplasm collection: tools for breeding programs and genetic conservation. Genetica, v. 147, n. 5, p. 359-368, 2019.
• GUÉNEAU, S.; DINIZ, J. D. A. S.; PASSOS, C. J. S. Alternativas para o bioma Cerrado: agroextrativismo e uso sustentável da sociobiodiversidade. Brasília, DF: IEB Mil Folhas, 2020.
• GUIMARÃES, R. A.; MIRANDA, K. M. C.; MOTA, E. E. S.; CHAVES, L. J.; TELLES, M. P. C.; SOARES, T. N. Assessing genetic diversity and population structure in a Dipteryx alata germplasm collection utilizing microsatellite markers. Crop Breeding and Applied Biotechnology, v. 19, n. 3, p. 329-336, 2019.
• JUSTINO, A. B.; MOURA, F. R. B. de; FRANCO, R. R.; ESPINDOLA, F. S. α-glucosidase and non-enzymatic glycation inhibitory potential of Eugenia dysenterica fruit pulp extracts. Food Bioscience, v. 35, e100573, 2020.
• MARTINOTTO, C.; PAIVA, R.; SANTOS, B. R.; SOARES, F. P.; NOGUEIRA, R. C.; SILVA, Á. A. N. Efeito da escarificação e luminosidade na germinação in vitro de sementes de cagaiteira (Eugenia dysenterica DC.). Ciência e Agrotecnologia, v. 31, n. 6, p. 1668-1671, 2007.
• MOTA, C. S.; ARAÚJO, E. L. S.; SILVA, F. G.; DORNELLES, P.; FREIBERGER, M. B.; MENDES, G. C. Physiology and quality of Eugenia dysenterica DC seedlings grown in vermiculite and rice husk-based substrates. Revista Brasileira de Fruticultura, v. 40, n. 1, p. 49-58, 2018.
• MYERS, N.; MITTERMEIER, R. A.; MITTERMEIER, C. G.; FONSECA, G. A. B. da; KENT, J. Biodiversity hotspots for conservation priorities. Nature, n. 403, p. 853-858, 2010.
• NOVAES, C. R. D. B.; MOTA, E. E. S.; NOVAES, E.; TELLES, M. P. C.; CHAVES, L. J. Structure of the phenotypic variability of fruit and seed traits in natural populations of Eugenia dysenterica DC. (Myrtaceae). Revista Brasileira de Fruticultura, v. 40, n. 3, p. 843-854, 2018.
• NUNES, H. V.; BARROS, D. I.; SANTOS, J. P. P. dos; OLIVEIRA, K. R. D. S. de; BARBOSA, B. A.; NUNES, B. H. di N.; NOLETO, R. F.; COSTA, G. H. A.; MIRANDA, C. P.; VALE, K. C. L.; OLIVEIRA, L. B. de. Vigor and viability of cagaita (Eugenia dysenterica DC.) seeds subjected to different substrates. European Journal of Medicinal Plants, v. 31, n. 10, p. 52-56, 2020.
• OGA, F. M.; FONSECA, C. E. L. Um método rápido para estimar área foliar em mudas de cagaiteira (Eugenia dysenterica D.C.). Pesquisa Agropecuária Brasileira, v. 29, n. 4, p. 571-577, 1994.
• OGA, F. M.; FONSECA, C. E. L.; SILVA, J. A. Influência da profundidade de semeadura e luminosidade na germinação de sementes de cagaita (Eugenia dysenterica Mart.). Revista do Instituto Florestal, v. 4, n. 2, p. 634-639, 1992.
• PADI, F. K.; OPOKU, S. Y.; ADOMAKO, B.; ADU-AMPOMAH, Y. Effectiveness of juvenile tree growth rate as an index for selecting high yielding cocoa families. Scientia Horticulturae, v. 139, n. 1, p. 14-20, 2012.
• PROENÇA, C. E. B.; GIBBS, P. E. Reproductive biology of eight sympatric Myrtaceae from central Brazil. New Phytologist, v. 126, n. 2, p. 343-354, 1994.
• R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2013.
• ROACH, D. A.; WULFF, R. D. Maternal effects in plants. Annual Review of Ecology and Systematics, v. 18, n. 1, p. 209-235, 1987.
• RODRIGUES, E. B.; COLLEVATTI, R. G.; CHAVES, L. J.; MOREIRA, L. R.; TELLES, M. P. C. Mating system and pollen dispersal in Eugenia dysenterica (Myrtaceae) germplasm collection: tools for conservation and domestication. Genetica, v. 144, n. 2, p. 139-146, 2016.
• SANTOS, H. G. dos; JACOMINE, P. K. T.; ANJOS, L. H. C. dos; OLIVEIRA, V. Á. de; LUMBRERAS, J. F.; COELHO, M. R.; ALMEIDA, J. A. de; ARAÚJO FILHO, J. C. de; OLIVEIRA, J. B. de; CUNHA, T. J. F. Sistema brasileiro de classificação de solos 5. ed. Brasília, DF: Embrapa Solos, 2018.
• SCHEPPER, V. D.; DUSSCHOTEN, D.V.; COPINI, P.; JAHNKE, S.; STEPPE, K. MRI links stem water content to stem diameter variations in transpiring trees. Journal of Experimental Botany, v. 63, n. 7, p. 2645-2653, 2012.
• SILVA, S. R. D.; DOURADO, W. D. S.; NAVES, R. V.; VIEIRA, M. D. C.; PEREIRA, C. C. D. O.; SOUZA, E. R. B. D. Desenvolvimento de mudas de Eugenia dysenterica (Mart.) DC. no Cerrado de Goiânia. Revista de Ciências Agrárias, v. 40, n. 4, p. 40-49, 2017.
• SOUZA, E. R. B.; CARNEIRO, I. F.; NAVES, R. V.; BORGES, J. D.; LEANDRO, W. M.; CHAVES. L. J. Emergência e crescimento de cagaita (Eugenia dysenterica D.C.) em função do tipo e do volume de substratos. Pesquisa Agropecuária Tropical, v. 31, n. 2, p. 89-95, 2001.
• SOUZA, E. R. B.; NAVES, R. V.; CARNEIRO, I. F.; LEANDRO, W. M.; BORGES, J. D. Crescimento e sobrevivência de mudas de cagaiteira (Eugenia dysenterica DC) nas condições do Cerrado. Revista Brasileira de Fruticultura, v. 24, n. 2, p. 491-495, 2002.
• SOUZA, E. R. B.; NAVES, R. V.; OLIVEIRA, M. F. I. Início da produção de frutos de cagaiteira (Eugenia dysenterica DC) implantada em Goiânia, Goiás. Revista Brasileira de Fruticultura, v. 35, n. 3, p. 906-909, 2013.
• SWARUP, S.; CARGILL, E. J.; CROSBY, K.; FLAGEL, L.; KNISKERN, J.; GLENN, K. C. Genetic diversity is indispensable for plant breeding to improve crops. Crop Science, v. 61, n. 2, p. 839-852, 2021.
• TOMLINSON, K. W.; STERCK, F. J.; BONGERS, F.; SILVA, D. A.; BARBOSA, E. R. M.; WARD, D.; BAKKER, F. T.; KAAUWEN, M. V.; PRINS, H. H. T.; BIE, S.; LANGEVELDE, F. V. Biomass partitioning and root morphology of Savanna trees across a water gradient. Journal of Ecology, v. 100, n. 5, p. 1113-1121, 2012.
• TRINDADE, M. G.; CHAVES, L. J. Genetic structure of natural Eugenia dysenterica DC (Myrtaceae) populations in northeastern Goiás, Brazil, accessed by morphological traits and RAPD markers. Genetics and Molecular Biology, v. 28, n. 3, p. 407-413, 2005.
• UNITED STATES DEPARTMENT OF AGRICULTURE (USDA). Soil Survey Staff. Keys to soil taxonomy 12. ed. Washington, DC: USDA-Natural Resources Conservation Service, 2014.
• VENCOVSKY, R.; CROSSA, J. Measurements of representativeness used in genetic resources conservation and plant breeding. Crop Science, v. 43, n. 6, p. 1912-1921, 2003.
• VENCOVSKY, R.; NASS, L. L.; CORDEIRO, C. M. T.; FERREIRA, M. A. J. F. Amostragem de recursos genéticos vegetais. In: NASS, L. L. Recursos genéticos vegetais Brasília, DF: Embrapa Recursos Genéticos e Biotecnologia, 2007. p. 193-229.

Publication Dates

• Publication in this collection
  01 Dec 2021
• Date of issue
  2021

History

• Received
  26 Apr 2021
• Accepted
  04 Aug 2021
• Accepted
  21 Sept 2021