ARTIGO CIENTÍFICO: A phenological scale for the development of Gladiolus

Annals of Applied Biology ISSN 0003-4746

RESEARCH ART I C LE

A phenological scale for the development of GladiolusN.T. Schwab, N.A. Streck, C.C. Becker, J.A. Langner, L.O. Uhlmann & B.S.M.R. Ribeiro

Departamento de Fitotecnia, Centro de Cincias Rurais, Universidade Federal de Santa Maria (UFSM), Av. Roraima 1000, 97105-900 Santa Maria, RS, Brazil

Keywordsdevelopmental scale; developmental stages;oriculture; Gladiolus grandiorus;morphological criteria; phenology.

CorrespondenceN.A. Streck, Departamento de Fitotecnia, Centrode Cincias Rurais, Universidade Federal de SantaMaria (UFSM), Av. Roraima 1000, 97105-900,Santa Maria, RS, Brazil. Email:[email protected],[email protected]

Received: 20 January 2014; revised versionaccepted: 17 December 2014; published online:5 February 2015.

doi:10.1111/aab.12198

Abstract

A staging system for development of gladiola (Gladiolus grandiorus) that relieson simple, visual, non-destructive criteria is proposed. Four eld trials wereconducted during the spring 2010, autumn/winter 2011 and winter 2011 atSanta Maria, RS, Brazil, with different gladiola cultivars, in order to observethe developmental stages of the above-ground parts and their dry matter. Thedevelopmental cycle, which starts at dormant corm and ends with plant senes-cence, is divided into four developmental phases: dormancy phase, sproutingphase (from liform roots appearance to sheaths appearance), vegetative phase(from emergence of the rst leaf tip to emergence of the nal leaf tip on thestem) and reproductive phase (from heading to plant senescence). The develop-mental stages that were identied during the dormancy phase and during thesprouting phases are coded as S stages: S0 = dormant corm, S1 = appearance ofroots, S2.1=rst sheath, S2.2= second sheath and S2.3= third sheath. Vegeta-tive phase is coded as V stages: VE = emergence of the sheaths above ground,V1 = rst leaf, V2 = second leaf, Vn=nth leaf and VF = ag leaf. Leaf tip is themarker for V1VF. The developmental stages during the reproductive phasesare coded as R stages: R1 = heading, R2 = blooming, R3 = onset of owering,R4 = end of anthesis, R5 = end of orets senescence and R6 = plant senescence(leaves and oret axis are brown). Sub-stages have also been assigned betweenR1 and R2 and between R3 and R4. Illustrations (photographs) of each develop-mental stage taken from eld pot-grown plants are provided and the proposedscale was tested with eld observations. These criteria are straight forward andallow for quick determination of development stage. This system can be usedby both farmers and for experimental trials.

Introduction

Gladiola (also gladiolus) or sword lily (Gladiolus gran-diorus Hort.), Iridaceae family, is an important cut ower

propagated from corms. Gladiolus is considered the genus

within the largest known number of species of the

petaloid monocots, occurring naturally mainly in the

Mediterranean and Southern Africa regions, where there

are more than 100 wild species of Gladiolus (Greving,

1987; Tombolato et al., 2005; Riaz et al., 2010). The mar-

ketable ower of gladiola is botanically a one-sided spike

with many orets. The owers of cultivars come in a

variety of colours. In addition to a cut ower, the beau-

tiful blossom of gladiola may also be used in owerbeds

to create colourful gardens (cottage-style) such as in the

reconstructedMonets garden at Giverny, France (Willery,2010).

Even though gladiola are grown in many tropical, sub-tropical and temperate regions worldwide (Ahmad et al.,2011), detailed studies on the phenology of gladiola arescarce. Previous studies on gladiola phenology is dedi-cated primarily to describing below-ground development(Trinklein, 2005), whereas above-ground development isdescribed with fewer details (Cuevas, 1999). A detaileddescription of the above-ground development of glad-iola is important for basic studies on the biology andphenology of the species as well as for practical pur-poses, such as the timing of eld management practicessuch as nitrogen side-dressing, disease and insect con-trol and harvest scheduling (Greving, 1987; Smith, 2006).

496 Ann Appl Biol 166 (2015) 496507 2015 Association of Applied Biologists

Schwab et al. Staging system for describing the development of gladiolus

Therefore, a better understanding of gladiola phenologyhas the potential to improve ower quality and minimiseenvironmental effects on commercial production systems.

Phenology is the study of development (Hodges, 1991).Plant development can be dened as a process by whichindividuals or organs go through several identiablestages during their life cycle (Wilhelm&McMaster, 1995),and includes cell differentiation and organ initiation andappearance, and may extend throughout the plant lifecycle including senescence (Hodges, 1991; Wilhelm &McMaster, 1995). Meier et al. (2009a) dened phenologyas the study of the events in the life cycle of animals andplants, and these events are inuenced by environmen-tal factors. A developmental stage is usually characterisedby the appearance (morphogenesis) of an organ, whereasthe interval of time between two stages is dened as adevelopmental phase (Streck et al., 2003). An organ canbe identied using magnication (hand lens or micro-scope) or in some cases by the naked eye.

The description of plant developmental stages hasbeen of interest for centuries with records dating startingin A.D. 750 for the owering period of cherry trees inJapan (Morais et al., 2008). Once the relevant devel-opmental events in a plants life cycle are determined,their sequence can be assembled into a developmen-tal or phenological scale with stages designating thoseevents. Developmental staging systems are useful toolsto standardise communication among those involvedin agricultural activities such as farmers, consultants,extension agents, crop insurers, educators and scientistsand are an aid in providing crop management practices(Counce et al., 2000). Developmental scales have fourmain parts: the name of the developmental phases, thename of the developmental stages within each devel-opmental phase, a code (a number, a set of letters or acombination of letters and numbers) and a description(criteria) of each developmental stage (Zadoks et al.,1974; Fehr & Caviness, 1977; Counce et al., 2000).

Developmental scales have been proposed for severalagricultural crops, including annual grain crops such assoybean (Fehr & Caviness, 1977), maize (Hanway, 1966;Ritchie et al., 1993), wheat (Large, 1954; Zadoks et al.,1974) and rice (Counce et al., 2000), and fruit crops suchas persimmon tree (Garcia-Carbonell et al., 2002), olivetree (Snz-Corts et al., 2002), coffee tree (Morais et al.,2008) and mango tree (Delgado et al., 2011). Some oralcrops also have phenological scales such as Rosa sp. (Meieret al., 2009b) and Zinnia elegans (Gonalves et al., 2008).The BBCH (Biologische Bundesanstalt, Bundessorte-namt, CHemische Industrie) system includes a scale forbulb vegetables but not for bulb owers (Feller et al.,1995). Bulb vegetables (onion and garlic) are biennials,whereas bulb owers, including gladiola, are perennials

and they differ greatly in development, so the BBCHscale for bulb vegetables is not suitable for gladiola. Weare unaware of a comprehensive and adaptive stagingsystem for gladiola, which constituted the rationale fordeveloping a phenological scale for this oral crop.

With regard to the coding approach, we present astaging system for gladiola where the code is comprised bya letter and a number, following the widely used codingsystems of maize (Ritchie et al., 1993), soybean (Fehr &Caviness, 1977) and rice (Counce et al., 2000), whereletters represent the developmental phase and numbersrepresent the developmental stage. This approach is easierfor end users such as extension agents and growers thana system coded only with numbers such as the Zadoksscale (Zadoks et al., 1974) and the BBCH system (Meieret al., 2009a).

The objective of this study was to create a stagingsystem for describing the development of gladiola thatrelies on simple, visual and non-destructive criteria thatare easy-to-use.

Materials and methods

A plant development system needs four main features(Counce et al., 2000): (a) dichotomous criteria based onplant morphogenesis (i.e. discrete morphological criteriawhich are either present or absent) to identify develop-mental stages and phases; (b) a basis on actual eventsrather than indications; (c) a wide range of geographicalapplication and (d) visible criteria ormarkers readily iden-tiable with a small hand lens (about 10magnication).Further, a staging system should have vegetative develop-ment based on cumulative leaf number (CLN), which is abiologically sound way to express plant age (Counce et al.,2000). The Hauns system (Haun, 1973) was the rst stag-ing system to formally incorporate CLN as a continuousdevelopmental stage for wheat. Fehr & Caviness (1977)incorporate CLN as V stages (vegetative stages) in theirsoybean system recognizing that the vegetative develop-ment can overlap the reproductive development. We con-sidered all the above requirements in the development ofour system for gladiola.

We followed the approach proposed by Counce et al.(2000) for developing a rice staging system. In laboratoryand eld experiments, we observed the developmentof gladiola corms and plants, and recorded progressionof phenological events. We also studied the literatureand discussed with scientists in biology and oriculturein order to determine the appropriate developmentalphases and stages. As the developmental stages weredened, at least two individuals made observations onthe plants in the experiments. If the criteria were notclear (dichotomous and objective), difcult to see or were

Ann Appl Biol 166 (2015) 496507 497 2015 Association of Applied Biologists

Staging system for describing the development of gladiolus Schwab et al.

interpreted differently by other observers, we discussedthe criteria until consensus was reached.

Gladiola morphogenesis was divided into four phases:corm dormancy, bud sprouting, vegetative and reproduc-tive. The developmental stages of the sprouting phasewere observed in ve commercially vernalised corms ofcultivar Jester, kept in a laboratory, in dark conditions andtemperature of 2530C, which were laid on a wet cottonmesh (January 2012). As the developmental stages werereached, the corms were photographed.

For documenting each of developmental stages of thevegetative and reproductive phases, commercially ver-nalised corms of cv. Jester were planted in 3.5-L potsand the potted plants grew in open eld conditions atSanta Maria, RS, Brazil (latitude 294323S, longitude534315Wand altitude 95m), from July 2011 to Febru-ary 2012. When the developmental stages were reachedon these potted plants, they were immediately pho-tographed.

Additionally, developmental stages of the vegetativeand reproductive phases were observed in three eldtrials conducted at the Departamento de Fitotecnia ofthe Universidade Federal de Santa Maria in Santa Maria,RS, Brazil. The rst trial was carried out from 8 Septem-ber 2010 to 29 December 2010 with seven cultivars:T704 (purple), Traderhorn (red), Sunset (yellow), Jester(yellow and red), Priscilla (pink and white), Peter Pears(orange) and Rose Supreme (pink). The seven gladiolacultivars are commonly grown and representative of thewide range of colours and developmental cycles of glad-iola cultivars used in Brazil. The second trial was carriedout from 30 March 2011 to 31 December 2011 usingthree cultivars: Traderhorn, T704 and Jester. In thesetwo trials, observations were made on ve plants of eachcultivar. The third trial was carried out from 5 August2011 to 8 April 2011 using three cultivars (Peter Pears,T704 and Jester) and observations were performed on24 plants of each cultivar. All three trials with plantingsat different times of year allowed for evaluation of thecriteria and ensured consistency for each developmentalstage of the scale.

In these eld trials, commercially vernalised cormswere planted in beds with two rows, 40 cm among rowsand 20 cm among plants within the rows. There were 10corms per cultivar in the rst two trials and 40 corms percultivar in the third trial. Agronomic practices used bylocal growers were used during the trials, which includedfertilisation, weed control by hoeing, irrigation and sup-porting plants vertically with individual bamboo stakesin the rst and second trials and with plastic net in thethird trial. Plants were observed daily and the dates ofoccurrence of the developmental stages were noted. Thecriteria selected to the identication of the developmental

stages had to be straight-forward and quick in the eld.While observing the plants, researchers made notes aboutthe difculties in applying the criteria to each stage ofdevelopment.

A fourth trial with Jester corms planted on 14 Septem-ber 2012 was conducted in Santa Maria, RS, Brazil, inorder to determine dry matter accumulation at eachdevelopmental stage of the development cycle of glad-iola. Corms were planted in a 10m bed in the sameplant spacing and management practices used during theprevious trials. Plants were observed daily and ve plantswere randomly sampled when they reached each devel-opmental stage. The soil was removed from the corm androots by washing them with tap water. Sampled plantswere separated into leaves, old corm, new corm, cormels,liform roots, contractile roots and oral stem, whichwere then oven dried at 60C. Dry matter distributionamong the different parts was calculated as a percentageof total dry matter at each developmental stage.

Results

The developmental scale for Gladiolus is presented inTable 1. Images of each developmental stage are presentedin Figs 17.

The dormancy phase is visible as a dormant cormwhichis not yet sprouted (Stage S0, Fig. 1A). There are fourstages within the sprouting phase: S1 (Fig. 1B), S2.1(Fig. 1C), S2.2 (Fig. 1D) and S2.3 (Fig. 1E). In the eld,the developmental stages of the sprouting phase occur inthe soil.

The vegetative phase starts when the shoot (usuallycomposed of three sheaths) emerges from the soil sur-face. Vegetative developmental stages are designated asV stages, beginning at VE (emergence of the sheathsabove the ground) and extend until the last leaf (herecalled the ag leaf as in other monocots) is visible. AfterVE, the number in the code denotes the number of true(foliage) leaves above the last sheath, i.e. the CLN, sothat a plant at V1 has one leaf, V2 two leaves and so forthuntil the nal (ag) leaf is visible (VF). The marker forV1VF is when the leaf tip is visible to the observer, i.e.the leaf tip appearance. Images of plants at VE, V1, V2,V3, V6 and VF are in Fig. 2A, 2B, 2C, 2D, 2E and 2F,respectively.

The reproductive phase starts in the proposed stagingsystem when the spike is rst visible at the whorl andends when the whole plant senesces. Developmentalstages are denoted as R stages. Heading (when the tipof the spike is visible at the whorl), blooming (whenorets show the colour of the corolla), anthesis (oretsare opening and anthers are visible) and orets senes-cence (when the corolla dehydrates and dies) are major



Table 1 The developmental staging system for Gladiolus

Phase Stages Code Description

Dormancy Dormant corm S0 Buds and root nodules are at rest and covered by the husks that overlap eachother covering the corm and meeting at the top of the corm

Sprouting Appearance of roots S1 Roots start growing from root nodules at the base of the corm

First sheath S2.1 The rst sheath that grew from the apex is visible at the top of the corm pushingup the husks

Second sheath S2.2 Sheath continues its growth through the husks and the second sheath is visibleat the top of the corm

Third sheath S2.3 Third sheath is visible at the top of the corm

Vegetative Emergence VE Shoot is rst visible above the ground

First leaf V1 First true leaf tip is visible at the shoot whorl

Second leaf V2 Second true leaf tip is visible at the shoot whorl

Third leaf V3 Third true leaf tip is visible at the shoot whorl. Florets differentiation starts at theapex (R0)

Nth leaf Vn Nth true leaf tip is visible at the shoot whorl

Flag leaf VF Last leaf tip is visible at the shoot whorl

Reproductive Heading R1.0 Spike tip rst visible at the shoot whorl

R1.1 Half of the spike emerged. The tip of the spike is level with the tip of the last leaf

R1.2 Emergence of spike completed. The peduncle of the spike is visible. After R1.2,the rachis elongates and orets grow apart

Blooming R2 First three orets at the bottom of the spike show the colour of the corolla. Thisis the marketable harvest point

Onset of anthesis R3 The corolla of the rst oret at the bottom on the spike is open with visibleanthers

Half of anthesis R3.4 The corolla of the oret located at the middle portion of the spike is open withvisible anthers

Beginning oret senescence R3.5 First oret at the bottom of the spike starts senescence (corolla of the rst oretis dehydrated)

Half of orets senesced R3.6 Floret at the middle of the spike starts senescence

Anthesis completed R4 The corolla of the last uppermost oret on the spike is open with visible anthers

End of oret senescence R5 Last uppermost oret on the spike senesced. Corolla of all orets are dead

Plant senescence R6 Above ground parts of the plant (leaves and oral axis) are brown (dead plant)

developmental stages, with some divisions within them

(Table 1). Images of plants at R1.0, R1.1 and R1.2 are in

Fig. 3A, 3B and 3C, and at R2 and at R3 are in Fig. 4A

and 4B, respectively. As the orets continue to open

upwards on the spike after R3 and when the oret at the

middle position of the spike is open, the plant is at R3.4

(Fig. 5A). When the rst oret at the bottom of the spike

starts to senesce, the plant is at R3.5 (Fig. 5B). When the

oret at the middle position of the spike senesces, the

plant is at R3.6 (Fig. 5C). Floret opening continues on

the spike until the last oret opens (R4, Fig. 6A) and the

oret senescence continues until the last oret senesces,

at R5 (Fig. 6B). At the end of the developmental cycle,

the whole plant has senesced, i.e. all leaves and oral

axis are brown. This is the stage R6 (Fig. 6C).

The total developmental sequence is presented in

Fig. 7. The morphological criteria for R1.0, R1.1 and R1.2

stages and the orets differentiation stage (R0) at V3

are shown in detail in Fig. 7. However, its identication

is only possible by dissecting the plant and observing it

under a magnication of 14 with a hand lens, as theapex is only about 6mm in length (Shillo &Halevy, 1976).

The number of days after planting to reach each devel-opmental stage of the vegetative phase (V stages) and thereproductive phase (R stages) in plants of the eld trialsare in Tables 24. In the rst trial (planting on 8 Septem-ber 2010), the stages R1.1, R1.2, R3.4, R3.5, R3.6, R5 andR6 were not observed (Table 2). In the second trial (plant-ing on 30 March 2011), the stages R1.1, R1.2, R3.4, R3.6,R5 and R6 were not observed (Table 3) and in the thirdtrial (planting on 5 August 2011) only the R3.6 stage wasnot observed (Table 4). The missing stages in the trialswere because, at that time, we were constructing the scaleand those developmental stages had not been dened yet.

The time (in days) from planting to each developmentalstage varied with cultivar (Tables 24). For instance, themarketable harvest time (stage R2) varied from 81 daysfor cultivar Priscilla to 97 days for cultivar Jester in the rsttrial (Table 2). Among planting dates, for cultivar Jester,the R2 was the shortest (95 days after planting) in thethird trial (Table 4) and the longest in the second trial



A B C

D E

Figure 1 Developmental stages during the dormancy and sprouting phases in Gladiolus: S0=Dormant corm (A), S1= appearance of roots nodules at the baseof the corm (B), S2.1=rst sheath (C), S2.2= second sheath (D), S2.3= third sheath (E). The circles indicate the root nodules (B) and the sheaths (CE). Thearrow in the insets of panels (D) and (E) indicates the liform roots at the base of the corm.

(122 days after planting) (Table 3), indicating strong effect

of temperature on the rate of development.

Drymatter distribution among different plant parts (old

corm, new corm, roots, leaves and spike) changed with

development stage (Fig. 8). From emergence to V3, about

80% of the plant dry matter is in the old corm (7.7 g

corm1) and from V4 forward the reserves in the old

corm have all been used. Florets differentiation and spike

growth starts at V3, spike starts an intense linear growth

at V7 and leaf dry matter is maximum at VF (V8 in Fig. 8)

(15.4 g plant1). At R3R4, spike dry matter is maximum

(17.3 g plant1) and about 80% of the total plant dry

matter (43.1 g plant1) is in leaves and spike. Filiform

roots are active until V4 and contractile roots start to

grow from that stage. Cormels usually start their growth

at R1 (it may vary among genotypes) and represent about

2% of the total plant dry matter at R5. The new corm

starts to grow at V1 but its growth is small until R5 (2.6 g

plant1). After R5, the growth of the new corm increases(18.6 g plant1) because all photoassimilates produced byleaves are translocated to below ground parts, until leavessenescence (R6).

Discussion

During the dormancy phase (S0, Fig. 1A), the cormremains dormant due to growth inhibitors, such asabscisic acid (ABA). This strategy allows the survival ofthe structure under adverse eld conditions, such as coldtemperatures and low soil moisture (Tombolato, 2004).The corm dormancy in gladiola can be broken by coldstorage (5C) or by applying growth regulators (Castroet al., 1970; Vidalie, 1990).

The sprouting phase initiates when the corm is plantedin the soil and liform roots start to grow from rootnodules at the base of the corm (S1, Fig. 1B). Then,



A B C

D E F

Figure 2 Developmental stages during the vegetative phase of Gladiolus: VE= emergence (A), V1=rst leaf (B), V2= second leaf (C), V3= third leaf (D)(the detail in V3 is the oret differentiation R0), V6= sixth leaf (E) and VF=ag leaf (F).

sprouting takes place in the upper part of the corm, and

the root growth continues, concurrently with the sheath

(incomplete leaves or bracts) growth (insets of Fig. 1D

and 1E). Leaf primordia differentiate at the apex of the

bud and usually three leaf sheaths grow from the bud

to protect the growing true leaf. It is possible that some

plants may have a fourth sheath and in this case the stage

would be coded as S2.4.

The vegetative phase contains a set of V stages, starting

at emergence (VE), suggesting that vegetative develop-

ment occurs by the accumulation of one leaf after the

other on opposite sides of the shoot (Fig. 2). At VE, usu-

ally one or two bracts of the three are visible above the

soil surface (Fig. 2A). Emergence is an important develop-

mental stage in many phenological systems (Zadoks et al.,

1974; Fehr & Caviness, 1977; Counce et al., 2000) because

it represents the beginning of leaf area growth and

therefore the beginning of solar radiation interception by

the canopy for photosynthesis.

During the vegetative phase, the period between theappearance of successive leaf tips upwards on the shoot isone phyllochron and can be easily determined by nakedeye. Photoassimilates during the vegetative phase areused to grow roots, the new corm and cormels, and thespike. An important eldmanagement practice in gladiolaoccurs at the V3 stage. Nitrogen is side-dressed at V3because oral differentiation starts at this stage inside thewhorl and is a strong nitrogen sink in the plant (Shillo& Halevy, 1976). Differentiation of orets is acropetaland the spike is visible at the whorl, right before the lastuppermost leaf tip (ag leaf) is visible (Fig. 2F), when thenal leaf number is dened, indicating that the vegetativephase has ended.

The reproductive phase is composed of a set of Rstages, starting with R1.0 (Fig. 3A). At this stage, it isimportant that plants are supported either with indi-vidual stakes (wood or bamboo-made) or with a plasticnet so that plants do not tilt or lodge as the peduncleof the spike elongates above the uppermost leaf (nal



A B C

Figure 3 Development of the spike during the reproductive phase in Gladiolus: R1.0= spike rst visible at the whorl (A), R1.1=half of the spike emerged fromwhorl (B), R1.2= emergence of spike is completed (C).

A B

Figure 4 Development of the spike during the reproductive phase in Gladiolus: R2=rst three orets at the bottom of the spike show the colour of the corolla(A), R3= the corolla of the rst oret at the bottom of the spike is open with visible anthers (B).

leaf number) and becomes heavy. When gladiola arepart of owerbeds (Willery, 2010), lodging is usuallynot a problem as neighbour plants support the gladiolaplant.

Following heading, the rachis elongates, the distanceamong orets increases and orets become obvious.Flowering occurs acropetally and at some point in timethe corolla of the rst oret shows colour. In commercialcut ower plantations, the R2-stage (Fig. 4A) is the rec-ommended harvest point for the spikes as it allows longvase life during transportation and marketing. Whencustomers see the spikes, three orets are usually open-ing. In Brazil, a major holiday for gladiola consumption isAll Souls Day (2 November). In order to have marketableowers for this holiday, planting is usually carried out

during the second half of July, V stages occur from endof August to mid-October and R3 has to occur 24 daysbefore the holiday.

When the corolla of the rst oret at the bottom ofthe spike is open, the stage indicates the onset of anthe-sis. In the Jester cultivar, the beautiful yellow corollais irregularly amed with red, and is rst visible at R3(Fig. 4B). Anthesis and senescence of the orets proceedupwards on the rachis until the uppermost oret has itscorolla open with visible anthers (Fig. 6A) and bloomingends. When the corolla of the uppermost oret senesces(Fig. 6B, after R5), the vase life has ended but the planthas green leaves, and photoassimilates are translocatedfrom the leaves to the new corm and cormels. A gladi-ola plant reaches the end of the cycle when the leaves



A B C

Figure 5 Development of the spike during the reproductive phase in Gladiolus: R3.4= the corolla of the oret located at the middle portion of the spike is openwith visible anthers (A), R3.5=rst oret at the bottom of the spike starts senescence (B), R3.6=oret at the middle of the spike starts senescence (C).

A B C

Figure 6 Development of the spike during the reproductive phase in Gladiolus: R4= the corolla of the uppermost oret on the spike is open with visible anthers(A), R5=uppermost oret on the spike senesced (B), R6= above ground parts of the plant have senesced (C).

Figure 7 Developmental sequence in Gladiolus. For description of developmental stages, see Table 1. The detail in V3 is the orets differentiation at the apex(R0), which is only possible to be seen under 14 magnication.



Table 2 Number of days from planting to developmental stages (DS) in seven Gladiolus cultivars planted on 8 September 2010 at Santa Maria, RS, Brazil. Eachvalue is the mean of ve plants and value in parenthesis is one standard deviation of the mean

Cultivars

DSa Priscilla Peter Pears Trader Horn Sunset Rose Supreme T704 Jester

VE 21 (3.69) 29 (7.11) 28 (2.57) 28 (4.64) 20 (0.99) 27 (1.41) 31 (3.33)VFb 78 (0.00) 78 (0.00) 94 (7.89) 86(0.00) 90(3.74) 91(5.29) 91(5.72)R1.0 72 (2.29) 78 (5.35) 83 (4.95) 82 (2.65) 87 (2.77) 85 (2.49) 88 (5.32)R2 81 (3.51) 87 (5.19) 92 (4.95) 91 (1.15) 96 (2.95) 94 (2.19) 97 (4.82)R3 85 (3.39) 89 (5.25) 95 (6.36) 91 (4.04) 98 (3.09) 96 (2.95) 100 (4.85)R4 93 (3.53) 102 (5.07) 107 (0.71) 105 (0.58) 111 (2.38) 106 (2.30) 109 (3.29)

aFor description of DS, see Table 1.bPriscila and Peter Pears cultivars had eight leaves and the other cultivars had nine leaves.

Table 3 Number of days from planting to several developmental stages inthree Gladiolus cultivars planted on 30 March 2011 at Santa Maria, RS, Brazil.Each value is the mean of ve plants and value in parenthesis is one standarddeviation of the mean

CultivarsDevelopmental

stagesa Jester Trader Horn T704

VE 24 (5.15) 19 (5.14) 21 (5.80)VFb 115 (5.47) 100 (17.04) 78 (7.23)R1.0 110 (8.92) 90 (14.28) 117 (10.84)R2 130 (10.71) 109 (13.50) 122 (18.61)R3 132 (10.89) 113 (12.60) 126 (19.91)R3.5 139 (7.51) 122 (13.67) 128 (17.79)R4 147 (8.08) 131 (7.08) 143 (17.46)

aFor description of developmental stages, see Table 1.bCultivar T704 had eight leaves and the other cultivars had nine leaves.

have completely died (leaves and oral axis are brown),coded as R6 stage (Fig. 6C). At this stage, translocationof assimilates to the new corm and the cormels ceasesbecause there are no more photosynthetically activeorgans. Thus, the maximum size of the corm and themaximum number of cormels are set at R6.

The period from about R3 to R4 is the vase life ofgladiola. The longer the R3R4 period the better forcustomers. Therefore, the search for cultivars with longerR3R4 period should be in the portfolio of desirable traitsin gladiola breeding programmes. The data on durationof R3 and R4 in Tables 24 are based on gladiola grownand left to ower in the eld. As a cut ower, the spike isremoved from the plant and kept in vase from about R3to R4, and orets open with the reserves accumulated inthe rachis before it was removed from the plant. Thus, weexpect a close relationship between the duration of theR3 and R4 phase in the eld with its vase life, modulatedby temperature.

The staging system proposed in Table 1 and illustratedin Figs 17 was tested in the three eld trails, wheregladiola plants of different cultivars grew in distinctmeteorological conditions. In the 2010 trial, vegetative

Table 4 Number of days from planting to several developmental of develop-mental stages in three Gladiolus cultivars planted on 5 August 2011 at SantaMaria, RS, Brazil. Each value is the mean of 24 plants and value in parenthesisis one standard deviation of the mean

CultivarsDevelopmental

stagesa Peter Pears T704 Jester

VE 21 (4.24) 24 (3.74) 20 (3.95)V1 24 (1.82) 31 (3.47) 27 (1.71)V2 35 (1.11) 42 (2.64) 39 (3.54)V3 45 (1.12) 51 (3.95) 50 (3.17)V4 54 (1.18) 59(2.68) 57 (2.51)V5 62 (1.31) 68 (3.46) 66 (3.59)V6 69 (1.22) 73 (6.81) 73 (3.61)V7 75 (0.85) 79 (7.28) 75 (1.75)V8 80 (1.95) 85 (6.72) 80 (1.36)VF 80 (4.81) 92 (9.85) 86 (2.76)R1.0 85 (2.27) 86 (4.21) 84(2.34)R1.1 86 (2.37) 87 (5.52) 87 (2.96)R1.2 89 (1.76) 90 (5.51) 88 (2.44)R2 95 (2.14) 96 (4.10) 96 (2.05)R3 97 (2.13) 98 (3.56) 98 (1.98)R3.4 98 (1.11) 99 (2.29) 102 (2.24)R3.5 99 (1.80) 99 (1.89) 102 (2.20)R 3.6 107 (2.67) 109 (1.72) 106 (1.22)R4 106 (2.36) 108 (2.42) 109 (0.71)R5 108 (0.76) 110 (2.03) 111 (0.92)R6 216 (5.23) 189 (25.65) 210 (14.35)

aFor description of developmental stages, see Table 1.

development occurred during mild temperatures inSeptember and October (1525C) while reproductivedevelopment took place during warm temperatures(3037C) in November and December. In the 2011 trial,vegetative development occurred under mild tempera-tures (2025C) during April, May and June, whereasreproductive development occurred under low temper-atures (515C), during July and August. In the thirdtrial, the vegetative development occurred from Augustto October, when temperatures were mild (1525C)and reproductive development occurred in November(2530C), except the period between R5 and R6, which



Figure 8 Dry matter distribution among different parts of a Gladiolus plant (cv. Jester) as a function of developmental stage and days after emergence (DAE).Planting date was 14 September 2012. Each point is the mean of ve plants.

occurred from December to March, under elevatedtemperatures (2535C). These trials provided a gooddata set to evaluate the criteria for identifying eachdevelopmental stage of the proposed staging system.

In our team, we had a total of six personnel who wentto the eld andmade the observations of the developmen-tal stages in the trials. In each visit, at least two individualsassessed the plants and independently evaluated the cri-teria. Overall, the personnel found that using the criteriawas easy and they could quickly determine all develop-mental stages. These results are important, as detailedexperiments where several developmental stages have tobe analysed can be very labour intensive. Another impor-tant feature for a developmental scale is that the criteriamust be clear and objective. The personnel who did theobservations unanimously agreed about clarity and theobjective nature of the descriptions provided in Table 1.This allows for consistency among observations.

The different planting dates in the three trials resultedin different durations of vegetative and reproductivestages (Tables 24). The average length was 62, 77 and64 days for the vegetative (VEVF) phase and 23, 40and 22 days for the reproductive phase (R1R5) in thetrials planted on 8 September 2010, 30 March 2011 and5 August 2011, respectively. The longer length of all thedevelopmental stages during the 30 March 2011 planting

was because plants grew during autumn and winter(AprilAugust) when the air temperature varied from1.1C to 31.7C. Plants in the other two plantings devel-oped during the warmest months (SeptemberMarch)when air temperature varied from 1.2C to 36.3C. Theseresults indicate that air temperature has an importanteffect on the rate of the development in gladiola, similarto other agricultural crops (Hodges, 1991; Wilhelm &McMaster, 1995; Streck et al., 2003).

The phyllochron varied from 2 to 12 days per leaf(Table 4). The four V1V4 leaves required more timethan the V5V8 leaves. The difference was related totemperature. The rst four leaves developed at meanair temperature of 16.3C, while the last four leavesdeveloped at mean air temperature of 19.6C. Similareffects of temperature on leaf appearance rate have alsobeen reported for other agricultural crops (Wilhelm andMcMaster, 1995; Streck et al., 2003).

Plant growth (dry matter accumulation and its parti-tioning among plant parts) is modulated by developmen-tal stages (Fig. 8). As plant development progresses, somegrowth processes are connected to specic developmen-tal stages. For instance, in gladiola during the vegetativephase, the majority of plant dry matter accumulates inthe leaves. At the V3 stage, the spike starts its growth andat the V4 stage the contractile roots start their growth,



whereas cormels only start their growth at R1 (Fig. 8).This dynamic relationship between growth and develop-ment is another example of the importance of having adetailed phenological scale for gladiola. We expect the drymatter partitioning pattern in Jester (Fig. 8) to be con-sistent with other commercial gladiola cultivars, as thevariability of the genotype-dependent traits of cormel drymatter and number of leaves per plant is small.

The development scale proposed in this paper is aneasy and practical eld scale, suitable for use by farmers aswell as by extension personnel for research purposes. Thescale was tested with seven widely grown commercialgladiola cultivars in Brazil (Table 24). These cultivarshave similar colours and morphological features as thosegrown in Europe and North America. Consequently, thedevelopmental scale (Table 1) works for a wide rangeof gladiola cultivars (Gladiolus grandiorus). The scalecomprises stages during different developmental phases,from sprouting, vegetative and reproductive phases,including the period of commercial interest to producersof cut owers (VER2) and extends to plant senescence(R6), based on discrete (dichotomously) naked eye mor-phological criteria. The vegetative development is basedon CLN and the system can be expanded to includethe development of the spike inside the whorls beforeappearance (R1). Floret differentiation (which occurs atV3, Fig. 2D) is coded as R0 so that early reproductivedevelopment (R0R1) overlaps part of vegetative devel-opment (V3VF). The partial overlap between vegetativeand reproductive development also happens in other agri-cultural crops such as wheat (Zadoks et al., 1974), soybean(Fehr & Caviness, 1977) and rice (Counce et al., 2000).

Acknowledgements

Authors thank Charles Patrick Oliveira de Freitas, Gio-vana Ghisleni Ribas and Jos Eduardo Wink for theirassistance with the eld experiments and Patricio OrozcoContreras for capturing images of the plants. This workwas supported by the Conselho Nacional de Desen-volvimento Cientco e Tecnolgico (CNPq), Proc. no.302524/2011-8, and by Coordenao de Aperfeioa-mento de Pessoal de Nvel Superior (CAPES).

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ARTIGO CIENTÍFICO: A phenological scale for the development of Gladiolus