A new approach towards the so-called recalcitrant seeds

Water is essential, irreplaceable, and indispensable for any kind of carbon-based-life metabolic activity. Water-dependent living beings are the expected pattern in nature. However, some organisms can survive for some time at a minimum water content, such as seeds of some species (orthodox seeds). Nevertheless, the expected standard life behavior is found in seeds of another group of species, the so-called recalcitrant seeds, which are sensitive to desiccation. A huge range of different behaviors can be found between these two groups, leading authors to consider that orthodoxy and recalcitrance is not an all-or-nothing situation. Notwithstanding, we are still too far from understanding the differences and similarities between all these kinds of seeds and this has been a serious barrier to the development of plant conservation technologies. A new approach to understanding the differences between these seeds is presented here based on seed maturation, environmental influences, and evolution. From this point of view, all kinds of seed behavior are contemplated and, consequently, some new perspectives are considered for the recalcitrant seed conservation technology, the most intensely desired technology nowadays in this area.

Index terms:
seed conservation; seed maturation; seed physiology

Authorship

Claudio José Barbedo ^**Corresponding author <claudio.barbedo@pesquisador.cnpq.br>

Instituto de Botânica, Núcleo de Pesquisa em Sementes, 04301-012 - São Paulo, SP, Brasil.Instituto de BotânicaBrazilSão Paulo, SP, BrazilInstituto de Botânica, Núcleo de Pesquisa em Sementes, 04301-012 - São Paulo, SP, Brasil.

^*Corresponding author <claudio.barbedo@pesquisador.cnpq.br>

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (6)
Tables (1)

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Figure 1
Distribution of the researches on recalcitrant seeds in Brazil, by area, in the period from 2010 to 2015.

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Figure 2
Seeds of species of the Brazilian flora. Surface of recalcitrant seed of Eugenia pyriformis covered by fungi of the genus Fusarium, Penicillium, and Ceratocystis (a); seeds of Caesalpinia echinata (brazilwood), an example of seeds highly tolerant to desiccation, but which remain viable for only a few months (b); raceme with fruits of Syagrus romanzoffiana at different maturation stages (c); seeds of Poincianella pluviosa, which has a long maturation period, but from a very early stage can disperse seeds with the capacity to germinate (d); seeds of Inga vera, which tolerate hypoxia conditions for several days (e); seeds of Eugenia cerasiflora, which have the capacity to produce roots and seedlings from cotyledon tissues: from left to right, seed drilled by insect larvae, damage caused internally by this insect, and seed fractioned into four parts, each of them producing a new seedling (f). Photos: C.F. Françoso, M.R. Bonjovani, D.M. Molizane, L.F. Delgado, V.A. Garcia, C.J. Barbedo.

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Figure 3
Variations in water content (A) and dry matter content and germination capacity (B) in seeds over maturation. Seed dispersion would occur at the end of the maturation drying, i.e., at the lowest value of water content. By mutation and natural selection processes, the species could change the traditional curve to one with an early dry matter accumulation, which may be due to an early dispersion, as indicated by the arrow (C). Standardized curves with generic behavior for species with classical orthodox seeds (B) could, therefore, be altered to adapt to the conditions of the environment in which each species is selected. The early maximum dry matter accumulation for an early dispersion (C) could require less investment in this accumulation, sacrificing part of the total amount to be accumulated. Thus, there would be a new pattern of dry matter accumulation for this species. This pattern could also undergo environmental action at each production cycle depending on the year and location. This action could further anticipate the moment of dispersion (D). However, the observer at this location and year would have access only to the information until the moment of dispersion (E) and could consider this the pattern of the species. Likewise, there could be variations in the acquisition of the germinative capacity (F). An even greater early dispersion would not affect the germinative capacity since its maximum was also much early (G), leading the observer to conclude that this is the maximum possible development for the species (H). This observation could be performed for all seed characteristics of that species, in that year and location (I).

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Figure 4
Hypothetical diagram of the environmental action on the reserve accumulation during seed maturation. The frontal observation by the age axis (X-axis) with the dry matter axis in the vertical (Y-axis) would produce a two-dimensional graph, characterizing the expected pattern for the species. The environmental variables (Z-axis) would alter this pattern, producing a response surface. The dry matter accumulation curve would be the result of traversing the standard curve on the Z-axis. Going through the back or front, we would have the oscillations in the dry matter accumulation of the same species in different years, or in different regions, i.e., the phenotypic variation. A cut-off plane at a given point, characterizing the conditions of the environment in a particular year and location, would show the resulting curve as a two-dimensional graph: if it is more in front, it will show an early accumulation in relation to a cut more in back, as illustrated in the two-dimensional graphs resulting from two cut-off planes of the response surface.

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Figure 5
Variations in water content, desiccation tolerance, and storage capacity (A) in seeds during their maturation. By mutation and natural selection processes, the species could dispense with the investment in prolonged storage (B) and desiccation tolerance (C), delaying the onset of these processes. The observer would only have access to the information until the moment of dispersion (D) and could consider this the maximum maturation potential of seeds of the species. The species could adopt this strategy to guarantee high germination rates already at the beginning of seed maturation (E, derived from Figure 3), perhaps due to an early dispersion in an environment favorable to colonization and highly competitive. Similar to the dry matter and germination curves, a new pattern of desiccation tolerance and longevity would be obtained and the observer of this species would consider the set of characteristics of the seeds dispersed as the pattern of a mature seed (E).

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Figure 6
Hypothetical diagram of the environmental action on the acquisition of desiccation tolerance during seed maturation. The frontal observation by the age axis (X-axis) with the desiccation tolerance axis in the vertical (Y-axis) would produce a two-dimensional graph, characterizing the expected pattern for the species. The environmental variables (Z-axis) would alter this pattern, producing a response surface. The desiccation tolerance curve would be the result of traversing the standard curve on the Z-axis. Going through the back or front, we would have the oscillations in the desiccation tolerance of the same species in different years, or in different regions, i.e., the phenotypic variation. These oscillations could also be obtained by applying special techniques of induction of desiccation tolerance such as osmoconditioning and application of reduced glutathione. A cut-off plane at a given point, characterizing the conditions of the environment in a particular year and location, would show the resulting curve as a two-dimensional graph: if it is more in front, it will show a high desiccation tolerance in relation to a cut more in back, as illustrated in the two-dimensional graphs resulting from two cut-off planes of the response surface. However, note that the oscillations did not allow reaching the high levels of the classical orthodox seeds.

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Table 1
Distribution of the researches carried out with recalcitrant seeds in the Brazilian and world literature based on a survey of the last 20 years of articles that contain the expression “recalcitrant seeds”. Source: Google/Scholar, July 2, 2018.

Figure 1 Distribution of the researches on recalcitrant seeds in Brazil, by area, in the period from 2010 to 2015.

Figure 2 Seeds of species of the Brazilian flora. Surface of recalcitrant seed of Eugenia pyriformis covered by fungi of the genus Fusarium, Penicillium, and Ceratocystis (a); seeds of Caesalpinia echinata (brazilwood), an example of seeds highly tolerant to desiccation, but which remain viable for only a few months (b); raceme with fruits of Syagrus romanzoffiana at different maturation stages (c); seeds of Poincianella pluviosa, which has a long maturation period, but from a very early stage can disperse seeds with the capacity to germinate (d); seeds of Inga vera, which tolerate hypoxia conditions for several days (e); seeds of Eugenia cerasiflora, which have the capacity to produce roots and seedlings from cotyledon tissues: from left to right, seed drilled by insect larvae, damage caused internally by this insect, and seed fractioned into four parts, each of them producing a new seedling (f). Photos: C.F. Françoso, M.R. Bonjovani, D.M. Molizane, L.F. Delgado, V.A. Garcia, C.J. Barbedo.

Figure 3 Variations in water content (A) and dry matter content and germination capacity (B) in seeds over maturation. Seed dispersion would occur at the end of the maturation drying, i.e., at the lowest value of water content. By mutation and natural selection processes, the species could change the traditional curve to one with an early dry matter accumulation, which may be due to an early dispersion, as indicated by the arrow (C). Standardized curves with generic behavior for species with classical orthodox seeds (B) could, therefore, be altered to adapt to the conditions of the environment in which each species is selected. The early maximum dry matter accumulation for an early dispersion (C) could require less investment in this accumulation, sacrificing part of the total amount to be accumulated. Thus, there would be a new pattern of dry matter accumulation for this species. This pattern could also undergo environmental action at each production cycle depending on the year and location. This action could further anticipate the moment of dispersion (D). However, the observer at this location and year would have access only to the information until the moment of dispersion (E) and could consider this the pattern of the species. Likewise, there could be variations in the acquisition of the germinative capacity (F). An even greater early dispersion would not affect the germinative capacity since its maximum was also much early (G), leading the observer to conclude that this is the maximum possible development for the species (H). This observation could be performed for all seed characteristics of that species, in that year and location (I).

Figure 4 Hypothetical diagram of the environmental action on the reserve accumulation during seed maturation. The frontal observation by the age axis (X-axis) with the dry matter axis in the vertical (Y-axis) would produce a two-dimensional graph, characterizing the expected pattern for the species. The environmental variables (Z-axis) would alter this pattern, producing a response surface. The dry matter accumulation curve would be the result of traversing the standard curve on the Z-axis. Going through the back or front, we would have the oscillations in the dry matter accumulation of the same species in different years, or in different regions, i.e., the phenotypic variation. A cut-off plane at a given point, characterizing the conditions of the environment in a particular year and location, would show the resulting curve as a two-dimensional graph: if it is more in front, it will show an early accumulation in relation to a cut more in back, as illustrated in the two-dimensional graphs resulting from two cut-off planes of the response surface.

Figure 5 Variations in water content, desiccation tolerance, and storage capacity (A) in seeds during their maturation. By mutation and natural selection processes, the species could dispense with the investment in prolonged storage (B) and desiccation tolerance (C), delaying the onset of these processes. The observer would only have access to the information until the moment of dispersion (D) and could consider this the maximum maturation potential of seeds of the species. The species could adopt this strategy to guarantee high germination rates already at the beginning of seed maturation (E, derived from Figure 3), perhaps due to an early dispersion in an environment favorable to colonization and highly competitive. Similar to the dry matter and germination curves, a new pattern of desiccation tolerance and longevity would be obtained and the observer of this species would consider the set of characteristics of the seeds dispersed as the pattern of a mature seed (E).

Figure 6 Hypothetical diagram of the environmental action on the acquisition of desiccation tolerance during seed maturation. The frontal observation by the age axis (X-axis) with the desiccation tolerance axis in the vertical (Y-axis) would produce a two-dimensional graph, characterizing the expected pattern for the species. The environmental variables (Z-axis) would alter this pattern, producing a response surface. The desiccation tolerance curve would be the result of traversing the standard curve on the Z-axis. Going through the back or front, we would have the oscillations in the desiccation tolerance of the same species in different years, or in different regions, i.e., the phenotypic variation. These oscillations could also be obtained by applying special techniques of induction of desiccation tolerance such as osmoconditioning and application of reduced glutathione. A cut-off plane at a given point, characterizing the conditions of the environment in a particular year and location, would show the resulting curve as a two-dimensional graph: if it is more in front, it will show a high desiccation tolerance in relation to a cut more in back, as illustrated in the two-dimensional graphs resulting from two cut-off planes of the response surface. However, note that the oscillations did not allow reaching the high levels of the classical orthodox seeds.

Table 1 Distribution of the researches carried out with recalcitrant seeds in the Brazilian and world literature based on a survey of the last 20 years of articles that contain the expression “recalcitrant seeds”. Source: Google/Scholar, July 2, 2018.

Central subject of the publication	Distribution according to the origin of the publication (%)
Central subject of the publication	Brazil	World
Desiccation tolerance	30	44
Storage	35	23
Cryopreservation	3	14
Ecology	5	5
Maturation	11	4
Germination	11	4
Other	4	6

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A new approach towards the so-called recalcitrant seeds

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[1] ^*Corresponding author <claudio.barbedo@pesquisador.cnpq.br>